Earth and life : global biodiversity, extinction intervals and biogeographic perturbations through time - Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence fromPrecambrian (Ediacaran) Weng’an and Early Cambrian Maotianshan Biotas,

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian (Ediacaran) Weng’an and Early Cambrian Maotianshan Biotas, China Jun-Yuan Chen

Abstract

Late Proterozoic (Ediacaran) Weng’an (580 mya) and Early Cambrian Maotianshan (c. 530 mya) faunas of South China, illustrated here, document diverse body plans at phylum and subphylum level and confirm that bilaterians evolved well before the “Cambrian explosion”. The Weng’an faunas (from Guizhou), the oldest record of metazoans, consist mainly of embryos with possible affinities to living sponges, cnidarians, and bilaterians, but with adult specimens (though microscopic) of the same groups. The Maotianshan Shale faunas (from Yunnan), remarkably diverse at species level (over 100 species), have great diversity of metazoan body plans, many comparable with those of living groups. Because they occur at or near the evolutionary roots of many animal groups, intermediate forms are present. Evolution of Early Cambrian metazoans was surprisingly rapid. Worm-like ancestral euarthropods elucidate the evolutionary origins of the arthropods. The diverse Maotianshan vertebrates, representing “missing” history between an amphioxus-like ancestor and craniate vertebrates, provide an improved understanding of the early evolution of the vertebrates. Keywords

China • Guizhou • Yunnan • Chengjiang • Latest Precambrian (Ediacaran)– Early Cambrian • Doushantuo Formation • Weng’an phosphate member • Fossil embryos • Maotianshan Shale (Early Cambrian) • Panarthropod phylogeny • Origin of Chordata and vertebrates (Cristozoa) • Inception of vertebrate brain • Phylogeny of Deuterostomia

Introduction J.-Y. Chen () LPS Institute of Geology and Palaeontology of Academia Sinica, Nanjing 210008, People’s Republic of China Institute of Evolution and Developmental Biology, Nanjing University, Nanjing 210093, People’s Republic of China e-mail: [email protected]; [email protected]

The sudden appearance of animal fossils at the beginning of the Cambrian was of particular concern to Darwin (The Origin of Species, 1859, pp. 313–314); it seemed to be at odds with his theory of evolution through natural selection. He believed that the Cambrian trilobites may have descended from

J.A. Talent (ed.), Earth and Life, International Year of Planet Earth, DOI 10.1007/978-90-481-3428-1_10, © Springer Science+Business Media B.V. 2012

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Precambrian ancestors long before the Cambrian. However, no Precambrian ancestor had yet been found at that time. The great evolutionary event called the Cambrian Explosion has been a great mystery and a highly controversial issue among researchers. Like a coin, the Cambrian explosion has two sides: the Cambrian above and the Precambrian below. The magnitude of the event can be understood based on the contrast between the biota and the degree of diversity of the fossils from both sides. Great advances have been made in Cambrian palaeontology over the past century (e.g., Whittington 1985), especially the discovery of the extraordinarily well-preserved soft-bodied fauna from the Middle Cambrian Burgess Shale (Briggs et al. 1994) and the Lower Cambrian Maotianshan Shale deposits (Chen 2004). The Cambrian side of the “Cambrian explosion” is richly illustrated and contrasts greatly with the Precambrian side, but it should be noted that with new finds, the diversity of both is increasing continuously. Compared with the Cambrian, our knowledge of Precambrian fossils is very limited. The discovery of the macroscopic Ediacaran biota in Australia in 1946 provided the first evidence of multicellular life before the Cambrian (Glaessner 1984). Members of the macroscopic Ediacaran biota are now found worldwide, and include enigmatic tubular and frondshaped sessile organisms. They emerged about 570 million years ago, flourished for a period of ca. 30 million years, and suddenly disappeared by the Precambrian/Cambrian transition 542 million years ago. The reasons for the extinction of the Ediacaran biota are not clear and are probably related to the advent of predators. The Ediacaran organisms have been described as metazoans with affinities to the Cnidaria (Glaessner 1959), molluscs (e.g. Kimberella Fedonkin and Waggoner 1997) and other bilaterians (Peterson et al. 2008), but most of the fossils are morphologically distinct from modern and even Cambrian life forms. Some palaeontologists do not agree that these creatures can be categorized using the currently accepted biological classification scheme (Seilacher 1989; Seilacher et al. 2003). Because it is difficult to deduce the evolutionary relationships among these Ediacaran organisms, some palaeontologists have suggested that they represent completely extinct lineages and established the kingdom Vendozoa (Seilacher 1984), now renamed the Vendobionta phyllum (Seilacher 1989). Because these

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enigmatic organisms predominantly left no descendants, the strange forms have been interpreted by some authors as “failed experiments” in multicellular life. The sudden appearance of metazoan diversity in the Cambrian with a great multiplicity of body plans in the animal groups at the phylum and subphylum levels remains a great mystery. Searching for metazoan fossils from Precambrian times is a challenging task. Once the efficient preservation of soft tissues, as well as bacteria (e.g. Bailey et al. 2007), in phosphate deposits was understood, palaeontologists began to look for metazoan fossils in Precambrian phosphate deposits. In 1998, two parallel teams found fossil embryos and sponges in the Precambrian Duoshantou phosphate deposit in Weng’an, Guizhou, southern China (Li et al. 1998; Xiao et al. 1998; Xiao and Knoll 1999, 2000). The Weng’an fauna, named after the fossil locality, is the oldest fossil record of metazoans and predominantly includes diverse embryos with affinities to living sponges, cnidarians, and bilaterians. In addition to the fossil embryos, the Weng’an fauna has yielded adult specimens of microscopic metazoans representing sponges, cnidarians, and bilaterians. The fauna lived in the early Ediacaran, immediately after the Snow Ball event, at least 580 million years ago, suggesting that metazoan life, including sponges, cnidarians, and bilaterians, flourished long before the Cambrian explosion and is indeed very deeply rooted. The great advances in Precambrian palaeontology, especially the intensive study of the Weng’an biota during the past 10 years, have significantly changed our view of the Cambrian explosion. However, the contrast between the Precambrian and Cambrian faunas remains great and the explosive Cambrian evolutionary event remains an enigma. The recently discovered fossil fauna from the Lower Cambrian Maotianshan Shale deposits in the Chengjiang, Haikou, and Anning areas near Kunming, China, documents the sudden appearance of a diversity of metazoans. These are not only remarkably diverse at the species level, including over 100 species, but illustrate a great morphological diversity of metazoan body plans. Many of these are comparable to those of living groups at the phylum and subphylum levels or were short lived and soon extinct (Gould 1989; Hou et al. 2004; Chen 2004). The close affinities between the 530-million-year-old Maotianshan Shale biota and the 505-million-year-old Burgess Shale biota suggest that

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these forms were geologically widespread and evolutionarily conserved following the Cambrian explosion. Because the intermediate forms were not well established and few survived, they appear only near the evolutionary roots of the related animal groups, becoming extinct soon after the new, advanced forms emerged. The fauna of the Maotianshan Shale lies close to the roots of many animal groups and intermediate forms living at that time. The discovery of many intermediate forms not only satisfies Darwin’s prediction but also casts new light on the evolutionary origins of the animal groups, especially the vertebrates and arthropods. The body plans (or body forms) of animals are essentially blueprints for the way the body of the organism is laid out (Raff 1996; Hall 1998; Chen 2009). The blueprint is shared by a group of animals ranked together at higher taxonomic levels, including superphyla, phyla, subphyla, classes, and orders. It is characteristic of a unique anatomical body organization that it is evolutionarily conserved and deeply rooted. The sudden appearance of the high animal diversity in the Cambrian corresponds to the sudden appearance of the diverse body plans of the animal groups at the phylum and subphylum levels. There are many living representatives of animals with these body plans, including vertebrates, ascidians, priapulids, sipunculans, arrow worms, possible molluscs, possible annelids, phoronida, and brachiopods (Chen 2004; Hou et al. 2004), many having changed little since the Cambrian (e.g. the ctenophores, priapulids, sipunculans, chaetognaths, tunicates, and inarticulate brachiopods). On the contrary, crest animals (the Cristzoa), including the extinct precraniates and living vertebrates (craniates), evolved rapidly and now include diverse and very distinct nested body plans that emerged later in evolution. The origin of the vertebrates has long been obscure and controversial, with a lack of fossil evidence for the first vertebrates and the very beginnings of vertebrate evolution. The fossils from the Maotianshan Shale, including Yunnanozoon, Haikouella, and Haikouichthys, are representatives of the missing history of early vertebrate evolution. The study of these fossils contributes to a new understanding of the evolutionary origin of the vertebrates, their heads, brains, head sensorial organs, branchial arches, backbones, and feeding behaviour.

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The limb-bearing segmented animals known as panarthropods have been diverse and abundant since the Early Cambrian and include diverse nested body plans representing different stages of evolution. Most of these different body plans appeared in the Early Cambrian, emerging one after another near the root of the evolutionary history of the panarthropods. Their appearance is a remarkable and rare phenomenon, shedding light on the evolutionary origins of various aspects of the arthropods, including the evolution of the head, limbs, and brain. The affinities of numerous Cambrian animals remain controversial. However, the body plans of these animal groups, especially the stalked sessile and pelagic medusiform lophophore-bearing animals and the vetulicolian organisms, offer clues to their possible affinities with extant animals. The regulatory network architecture is critical for establishing the body parts and body plan of the animals (Davidson 2006). The evolution of animal body plans provides us with interesting suggestions of how the genomic internal architectures and developmental processes that directed the course of evolution. The sudden birth of the diverse animal body plans suggests that the Cambrian explosion was marked with the diversification event of regulatory network architectures that regulate developmental processes of the animals.

The Oldest Fossil Evidence for the First Occurrence of Animal Life on Earth Molecular data predict that the divergence of the metazoans (including the calcisponges, cnidarians, and bilaterians) and the separation of the major bilaterian clades (the deuterostomes, ecdysozoans, and lophotrochozoans) occurred deep in time, either within the Ediacaran, following the Cryogenian Marinoan glaciation ending about 635 mya (Hoffman et al. 2004; Condon et al. 2005; Peterson and Butterfield 2005), or 100–200 million years before the Marinoan (Douzery et al. 2004). Recent discovery of possible sponge graded metazoan fossils in pre-Marinoan limestones from South Australia (Maloof et al. 2010) together with evidence from sponge biomarkers indicates that metazoans originated pre-Marinoan time, with a robust presence throughout the Ediacaran (Love et al. 2009).

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Fig. 1 Main localities producing the oldest known metazoans: the Wusi, Baishakan, and Nantuo quarries (adapted from Chen et al. 2009a)

Chen (2009) in discussing the appearance of diverse animal body plans during the Cambrian explosion states that “The Ediacaran Doushantuo phosphate deposits in Weng’an, Guizhou (Fig. 1) yield diverse metazoans, including sponges (Li et al. 1998), cnidarians (Chen et al. 2000, 2002a; Xiao et al. 2000), and bilateral animals and their related embryos (Chen et al. 2004b; Chen et al. 2006)”. This incredible 580-million-year-old Weng’an biota has received great attention because it is the oldest fossil evidence yet found for animal life on Earth.

Geological Setting of the Weng’an Biota The Doushantuo Formation is widely distributed in southern China and in areas of N. W. China. It is underlain by a glacial deposit known as the Nantuo Formation, laid down during the Marinoan glaciation and thus represents the first deposit after the last extensive glaciation of Snowball Earth. The Doushantuo Formation in Weng’an, Guizhou, crops out along the

axis of the Mt Beidou anticline (Fig. 1). It is well exposed in the Wusi quarry (Fig. 1), where the thickness is 49 m, consisting of five different lithological units (Fig. 2). The Weng’an phosphate member of the Doushantuo Formation varies laterally in thickness and lithology on a scale of metres to tens of metres (see Fig. 2). The Doushantuo Formation has been intensively quarried for phosphates at the Wusi, Baishaikang, and Nanbao quarries. All the specimens examined in the study come from the black and grey facies of the Weng’an phosphate member in these quarries. The quality of preservation varies among the three sites. Wusi (Fig. 3a) and Baishakan (Fig. 3b, c) are the best sites for metazoic embryos (Wusi and Baishakan) and microscopic adults (Baishakan). However, with extensive mining activity, these three quarries have suffered disastrous destruction by extreme sliding activity and have been deeply buried by massive rocks from the overlying strata (Fig. 3d, e). The Weng’an county government had recognized the fossil treasures at this site and erected a monument at the Baishakan quarry (Fig. 3c).

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Fig. 2 Natural and diagrammatic profiles of the lithologic sequence of the Ediacaran Doushatuo Formation in the Mt. Beiduoshan area, Wengan, Guizhou. The lithologic profile was photographed from the western part of the Baishakan quarry;

the thickness of lithologic units was measured in the Wusi quarry. WPM1 is the black facies, WPM2 the gray facies of the Weng’an Phosphate Member. MDM = Middle Dolomite Member; LPM = Early Phosphate Member

In the Yangtze Gorges area, about 600 km northeast of Weng’an (Fig. 2), the Lower Dolomite Member of the Doushantuo Formation, interpreted as a cap carbonate, contains an ash bed that has been dated as 635.23 ± 0.57 Ma using U–Pb dating techniques (Condon et al. 2005; Zhu et al. 2007). The top of the Doushantuo Formation in the Yangtze Gorges area contains another ash bed with a U–Pb age of 551.07 ± 0.61 Ma (Condon et al. 2005). Within the Doushantuo Formation at Weng’an, above the basal dolomite, are a lower and an upper phosphorite interval, separated by the Middle Dolomite Member with a minor hiatus above. The upper phosphorite interval, containing the rich Weng’an microfossil fauna, has been interpreted as younger than 580 million years by carbon isotopic and sequence stratigraphic analyses (Condon et al. 2005). However, the upper Doushantuo Formation corresponding to the Weng’an phosphate member has yielded a Pb–Pb age of 599 ± 4 (Barfod et al. 2002). A Pb–Pb age of 576 ± 14 million years has been calculated for the upper phosphate member (Chen et al. 2004a), providing additional evidence that the Doushantuo fauna predates the Ediacaran biota and is thus the oldest record of animal fossils currently

known. In summary, the balance of evidence indicates that the Doushantuo microfossils are older than 580 million years and hence are the earliest fossil assemblage displaying affinities to diverse metazoan groups.

Affinities of the Metazoan Embryos and Related Adults It is not easy to interpret the Doushantuo microfossils using traditional methods, either in petrographic thin sections (one per specimen) or with external scanning electron microscopy (SEM). Many of the microfossils, especially the embryos, are too simple in form to convey significant morphological information insofar as they resemble eggs or very early cleavage stages, although intriguing insights have been made into their early development (e.g. Chen et al. 2006). The diversity represented by these fossils has not yet been fully documented. A recent technological approach known as propagation phase contrast synchrotron X-ray microtomography (PPC-SR-μCT) provides a unique

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Fig. 3 Sites at the Wusi and Baishakan quarries producing the oldest known metazoans were well exposed several years ago but are now deeply buried by massive rock fall from the upper slope. A and B, photographed in 1997 and 2003, respectively, show well-exposed outcrops of the fossil-bearing beds in the Wusi (a) and Baishakan quarries (b) several years ago; (c), shows a

stone monument at the Baishakan quarry with illustrations of the Weng’an fauna about the evolutionary dawn of the animal life (photograph taken 2007); d and e show outcrops at the Wusi (d) and Baishakan quarries (e), now deeply buried by massive rocks shed from the upper slope (photographs taken by ZJ Yin in 2010)

analytical tool that is increasingly used in studying the Weng’an fossils (Chen et al. 2006, 2009a, b; Donoghue et al. 2006). Microtomography permits the non-destructive computational examination of specimens from any vantage point, the visualization of their internal characters in virtual sections in any plane, and virtual three-dimensional depictions of their internal structures. This technique reveals many structures that are invisible or barely visible with classical absorption contrast-based microtomography (Tafforeau et al. 2006; Chen et al. 2006, 2009a). In the case of the Weng’an fossils, it can show the complex internal features of structures that might previously have been ignored or misinterpreted because of their deceptive exterior forms (Fig. 4). Perhaps most importantly, it facilitates the analysis of the small minority of Doushantuo embryos that retain intrinsically complex structures and large numbers of cells.

The study of the Doushantuo microfossils was initially directed towards algae and acritarchs (Zhang 1989; Zhang and Yuan 1992) and intense interest has been generated in the metazoan embryos and adult forms since 1998 (Xiao et al. 1998; Li et al. 1998). The diversity of the animal forms represented in the microfossil assemblage and their possible phylogenetic affinities are increasing as our knowledge of the faunas continues to expand (Chen et al. 2000). More recently, great interest has been taken in the discovery of a microscopic putative adult bilaterian, Vernanimalcula (Chen et al. 2004a), with a general bilateral antero-posterior organization, a triploblastic structure, and bilateral symmetry. A pair of prominent coelomic structures lies symmetrically on each side of the prominent gut (Fig. 5). An anterior mouth is ventrally directed, followed by a thick pharynx with a multilayered wall and probable muscularity. The pharynx

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Fig. 4 PPC-SR-μT external view of a “soccer ball”-like 4-cell embryo (a) with chorionate cover consisting of large chorion cells (b); PPC-SR-μT is an external view of the chorionate cover

(c) and internal digital section (d) of an 8-cell embryo (adapted from Chen et al. 2009a)

opens posteriorly into a large stomach or intestine. The wall of the stomach or intestine is always composed of two tightly apposed, thin, phosphatized layers of tissue. These two layers are separated by a continuous thin partition, interpreted as the remains of a basement membrane. The endodermal layers bounding the stomach (or intestine) are continuous, with a thickened region of the external body wall at the posterior end, i.e. the anus (Fig. 5). Vernanimalcula is small but structurally complex, representing the earliest adult organism with a bilaterian form so far found in the fossil record. Its simple external morphology and lack of obvious appendages conform to the morphological and developmental predictions of the blueprint of an adult, triploblastic, coelomate animal.

The exquisite preservation of Vernanimalcula, however, has led some authors (e.g. Bengtson and Budd 2004) to suspect that these fossils are not real arguing that the authors “fail to take into full account taphonomy and diagenesis”. Chen et al. (2004c) believe that Bengston and Budd’s argument is not supported by sufficient evidence by counter-arguing that the open spaces in the animal, including its coeloms and the lumina of the mouth and oesophagus, are filled with black amorphous material derived from an organic sedimentary matrix that permeated through the pores of the fossilized wall of the animal while the sediment was still soft and hydrated (Fig. 5a). This indicates that the animal fossilization process began prior to the sediments becoming fully dehydrated. The firstgeneration cavity fillings in Vernanimalcula resulted

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Fig. 5 A–C, image in transmitted light (a), illustration (b), and restoration (c) of a microscopic bilaterian adult Vernanimalcula guizhouena from the Precambrian Doushantuo Formation, Weng’an, Guizhou, showing paired coeloms extending the length of the gut, syn-sedimentary organic micritic fillings in

the coeloms and late diagenetic vuggy fillings in the rear of the body. (d) a coelogastular embryo with possible cnidarian affinities showing organic micrite filling and whitish sparry diagenetic filling in shrinkage fractures (created by dewatering of internal sediments within the spacious blastocoel). Scale bar = 100 μm

from “internal sedimentation” while the matrix was still hydrated. The structures of Vernanimalcula were fossilized before internal cementation occurred, arguing against secondary diagenetic noise, and are primarily biological. However, early diagenesis did occur when the filling structure within the interspaces formed as the internal sediments dehydrated, and these usually appear between the fossilized biological wall and the internal sediments (Fig. 5a). A similar diagenetic history can be widely observed in the preservation of the Weng’an-type fossils. The early diagenetic products usually occur as a coating on either the outer or inner surface of the biological wall structure, as

diagenetic filling in the narrow interspaces formed by the dehydration of the sediments, or as internal sediments within the biological cavities. A later diagenetic product can also be seen in the specimens examined, as a clean, whitish dolomite filling the voids (Fig. 5a). The voids in the matrix and fossils were probably produced by freshwater dissolution in a late diagenetic stage, destructive in terms of fossil preservation. In addition to Vernanimalcula, the microscopic adult forms in the Weng’an fauna also include sponges, with a tabulate anthozoan form recorded in both thin section (Chen et al. 2002a; Xiao et al. 2000a, b) and with SEM (Xiao et al. 2000a, b) (Fig. 6b–f), and a

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Fig. 6 Microscopic cnidarian adults from the Precambrian Doushantuo Formation, Weng’an, Guizhou. (a, b) restoration (a) and transmitted-light photograph (b) of Eohydiania wenganense

(holotype); (c–f), restoration (c) and transmitted-light photograph (d–f) of coral-like cnidarian adult Sinocyclocylicus guizhouensis (Xue et al. 1992). Scale bar = 100 μm

hydroid-like form (Fig. 6a, b). Cross-sections of possible anthozoan polyps and stalks of similar sie and morphology have also been reported by Chen et al. (2002a) and Chen (2004), and exactly the same forms were discovered earlier by Xiao et al. (2000a, b). Microscopic (<1 mm) putative post-embryonic sponges have also been identified by the dense presence of acid-resistant monaxial spicules, irregular shape and filled with fossilized inclusions (Li et al. 1998; Fig. 7). In contrast to the rare preservation of adult forms, sub-millimetre embryos are a good size for phosphatization and are common and diverse in the

fauna. Many of the embryos retain a metazoan-like embryonic developmental sequence, but show no evidence of patterning organization or cell differentiation, even in the advanced stages of up to 2600 cells (Fig. 8). Their biological affinities remain enigmatic. Embryos displaying perfect radial symmetry with chorionated covers are common in the Weng’an biota. They are 600–800 μm in diameter. Embryos at the 8- and 16-cell stages have a central blastomere surrounded by peripheral blastomeres extending to the surface, and externally resemble a soccer ball (Fig. 9). These embryos are usually preserved with a

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Fig. 7 Microscopic sponges from Precambrian Doushantuo Formation, Weng’an, Guizhou, showing monoaxon spicules densely packed and irregularly arranged in adults (a, b) and late

developing embryos (c, d); preservation of possible sclerocytes at terminal end in some spicules (b, marked with arrow). Scale bar = 100 μm

chorion-like cover composed of tightly arranged, flattened cells, forming a regular reticulate pattern when viewed externally. Each cell retains a single depression, probably the original site of a cilium or flagellum. The embryos represent several different developmental stages up to the 32-cell stage. Thin sections show many samples of later developmental stages, with larger numbers of compacted blastomeres appearing to represent more advanced, late-cleavage sponge eggs.

Such forms were first recorded in 1998 and interpreted as possible bilaterians by Xiao et al. (1998). They have recently been re-interpreted as probable sponge embryos (Chen et al. 2009b) because similar embryos have been found in modern demosponges, as shown in SEM images (Leys and Ereskovsky 2006). Embryos with a one-cell-thick hollow gastrula are common in thin sections and an identically organized pattern of embryos has recently been documented

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Fig. 8 Embryos in different development stages showing no differentiation of the germ-layer. (a–c) transmitted light images at various stages of development; (d–f), PPC-SR-μT external view

of embryos at various stages of development. Sizes, 380 μm (a); 410 μm (b); 400 μm (c); 500 μm (d); 510 μm (e); 490 μm (f) (adapted from Chen et al. 2009b)

with PPC-SR-μCT technology. The highly organized, one-cell-thick, hollow gastrula displays a strong resemblance to the cnidarian (hydrozoan) gastrula in having a large blastocoel with several delaminated small cells on its floor (Fig. 10). The bilaterian-like embryos are not common and display diverse embryonic developmental patterns. Some of the embryos resemble bilaterian stereoblastulas undergoing epiboly, as seen in many living bilaterians, with a micromere cap at one end and large endoderm-like blastomeres at the other (Fig. 11). The micromeres in the micromere cap form an ectodermal covering extending down over the endodermal cells. However, a few are remarkable, showing a complex organization with polarities that are comparable to the anterior and posterior poles, dorsal and ventral poles, and left- and right-side symmetry seen in many modern bilaterian embryos. Ectoderm-like cells later appeared around the periphery on all but the ventral and ventrolateral surfaces of the embryo. The cells on both the ventral and ventrolateral surfaces are sub-spherical, suggesting that the external cap did not extend ventrally to cover them. Two highly organized 32-cell embryos also show a number of bilaterian characters, including the development of anterior–posterior, dorsal–ventral, and

right–left polarities (Figs. 12 and 13), and distinct, linearly aligned internal cells, densely packed with inclusions that represent the remains of yolk granules (Fig. 13). The putative yolky internal cells form a contiguous endodermal cord bent into a shallow “S” shape both laterally and ventrodorsally. The cord-like structure could be the precursor of the anterior–posterior gut, a bilaterian character. The organization of the presumptive ectoderm and endoderm in the embryo is not typical of any known animal. The disposition of the putative endodermal cord is unique insofar as it is exposed to the outside at both the anterior and posterior ends. Although the epibolic gastrulation of the large yolky eggs of many animal embryos terminates at a vegetal position, leaving some endodermal cells exposed (i.e. as a blastopore), there are two sites of endodermal exposure in no living animals. However, we should not be surprised that the embryos of the earliest animals are not exactly like those seen after 600 million years of evolution. In addition to the endodermal cord cells, there is a layer of smaller flattened cells that form what may be an ectodermal cap covering the dorsal and lateral surfaces of the embryo. The cells on the ventral surface are larger and subspherical, suggesting that the ectodermal layer may not have extended far enough ventrally to cover them.

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Fig. 9 Possible sponge embryos displaying perfect radial symmetry with chorionated cover (a–o) and a blastula in the modern demosponge (p). (a–h), transmitted light images of 2-cell (a, b), 4-cell (c, d), 8-cell (e, f), 16-cell (g), and possibly 64-cell (h) embryonic stages showing cellular nuclear (b, c) and perfect radial symmetry (e–h). (i–o) PPC-SR-μT images showing external (i) and internal views (j) of 16-cell embryo; external view (l) of a chorionated covered 8-cell embryo and a tangential slice (m)

through the chorion displaying the 3D nature of the chorion cell and a single depression in each cell (m); external view (n) and internal section (o) mid-way through a 16-cell embryo. P, SEM image of a blastula in the modern demosponge Halisarca dujardini (reproduced from fig. 8A in Leys and Ereskovsky 2006). Scale bars = 200 μm (a–h), 400 μm (i–l, n, o), 150 μm (m), and 40 μm (p)

Although composed of a relatively small number of cells, both of these fossil embryos display the complex organizational patterns and differentiated cell types seen in the early gastrulae of some existing invertebrates. The symmetrical and structural characteristics of the embryos suggest that they have anterior–posterior, dorsal–ventral, and right–left axes. The elongated embryo resembles a post-gastrulation bilaterian embryo, still in the last stage of gastrulation. Because of their large yolky eggs, cleavage stages seem similar in both embryos; the yolky endodermal cells are typically internalized by epiboly. During epibolic gastrulation, the presumptive ectodermal cells at

the animal pole of the embryo proliferate more rapidly than the yolk-rich endodermal cells and move in a vegetal direction to cover the endoderm. Despite similarities in their apparent modes of gastrulation, the spatial organizations of the cells of these two fossil embryos are clearly different. These major differences, in internal patterning and in right–left symmetry, suggest that rather than representing different stages of the developmental sequence of the same animal, these two embryos belong to two different animal taxa. This in itself shows that the stage of metazoan evolution represented by these Doushantuo specimens post-dates the last common bilaterian ancestor.

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Fig. 10 Fossil gastrula of possible cnidarian from Precambrian Doushantuo Formation, Weng’an, Guizhou. (a) PPC-SR-μT external view of blastopore; (b, c) successive digital internal sections of embryo in the same orientation—displaying several small cells on the floor of blastocoel (c); (d) a modern cnidarian gastrula showing small cells on blastocoel floor (reproduced from Pl XII, Fig. 56E of Mergener 1971). Scale bar = 150 μm (adapted from Chen et al. 2009a)

Fig. 11 Bilaterian embryos at late cleavage stage from Precambrian Doushantuo Formation, Weng’an, Guizhou. PPCSR-μT external view from micromere cap (a) and from the opposite (“endoderm”) side (b) and successive digital

sections displaying the larger endodermal blastomere cells (c) and micromeres (d); (e, f) PPC-SR-μT external view from micromere cap (e) and from the opposite, endodermal side (f). Scale bar = 250 μm (adapted from Chen et al. 2009a)

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Fig. 12 Postgastrular embryo from Precambrian Doushantuo Formation, Weng’an, Guizhou, displaying bilaterian characters including anterior, dorsal–ventral, and right–left polarities. (a) a PPC-SR-μT external view from right side along anterior (right)– posterior (left) axis, digital internal sections (b–d) and the same sections with cell boundaries drawn at reduced size, showing maximal dorsal–ventral asymmetry in section cut half-way from

right surface with flat ectodermal cells on dorsal, dorso-anterior and posterior surface (b); transitional state at section (c) with 30◦ rotation top-down away from observer from asymmetry (b); the plane of left-right bilateral subsymmetry at section (d) after 90◦ rotation from section B. Scale bar = 250 μm. Abbreviations: A, anterior; P, posterior; D, dorsal; V, ventral; R, right side; L, left side; ED, ectodermal cell (modified from Chen et al. 2009b)

The conclusion is consistent with other fossil studies and with the conclusions drawn from molecular phylogenetic analyses, placing the ancestor in the late Cryogenian, 635 million years or more ago, and hence before the end of Snowball Earth. Both types of embryonic developmental sequences appear to be similar to the duet spiral cleavage found in modern acoel flatworms (Boyer et al. 1996a). Quartet spiral cleavage with a giant polar macromere (Freeman and Lundelius 1992) is seen in the extant prostomian bilaterians, including many lophotrochozoans (Ax 1995) and crustacean ecdysozoans (Anderson 1975). Duet spiral cleavage patterning is characterized by the unusually early generation of micromere twins, beginning at the four-cell stage (Boyer et al. 1996b; Henry et al. 2000; Baguñà and Riutort 2004). The

cleavage division gives rise to the macromere twins forming the first two micromere twins. This is followed by the continuous cleavage of the micromere twins, producing macromere twins at the vegetal pole. These are capped with paired smaller micromere twins in the early-cleavage embryos. Numerous Doushantuo samples are similar to modern duet cleavage embryos, including several at different developmental stages, forming an early developmental sequence similar to that of extant acoel flatworms (Fig. 14a–h; Chen et al. 2009b). Quartet spiral cleavage establishes a micromere/ macromere pole, beginning at the eight-cell stage instead of the four-cell stage as in duet cleavage. D-quadrant specification is an early major developmental event in the establishment of the future axis of 

Fig. 13 (continued) section with cell boundaries drawn at reduced size, cut at 29% from the right surface, showing principal endodermal cells E4 and E1 sectioned near the right margin of the endodermal cord; (c) 35% from the right surface, showing endodermal cells E5, E4, and E1; (d) 43% from right surface. (e) 46% from right surface; (f) 51% from right surface; (g) 53% from right surface showing most parts of the endodermal cord close to the mid-plane of the embryo, and cluster of four cells, apparently daughter cells resulting from mitosis of E3; (h) enlarged E3. (i–j) digital external (i) and transparent view (j) from right side along the anterior (right: A) and posterior (left: P) axis showing anterior (AT) and posterior (PT) terminations (in red) of the putative endodermal cord of cells (i), and presumed ectodermal cells on dorsal surface, the putative endodermal cord

of cells (j, in red) that has a shallow S-shape dorso-ventrally, and extends through the embryo from anterior to posterior ends. (k, l) digital external (k) and transparent view (l) from dorsal side of the embryo showing cells at the anterior (AT) and posterior (PT) terminations of the putative endodermal cord (in red, k); the lines designated b–g represent locations of digital sections; the putative endodermal cord (red), is curved into a shallow S-shape laterally. Abbreviations: A, anterior; P, posterior; D, dorsal; V, ventral; L, left side; R, right side; ED, ectodermal cell; AT, anterior termination; and PT, posterior termination. Scale bar on left of H = 250 μm in digital sections (b–g), and 181 μm in H, 375 μm in A; sections with drawing of cell boundaries (at right-bottom), 250 μm in i–l (modified from Chen et al. 2009b)

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

Fig. 13 Postgastrular embryo from Precambrian Doushantuo Formation, Weng’an, Guizhou, displaying bilaterian characters: anterior (right)–posterior (left), dorso-ventral, and right–left polarities with putative yolky internal cells forming a continuous endodermal cord bent in a wide S-shape both laterally and

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dorso-ventrally. (a) PPC-SR-μT external view from dorsal side with lines (b–g) representing serial digital sections cut at successively deeper layers from the right surface, and the same sections with drawings of cell boundaries (at smaller size) with yolky internal cells (E1–E5) in red. (b) Internal section, and the same

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Fig. 14 Spiral cleavage embryos from Precambrian Doushantuo Formation, Weng’an, Guizhou. (a–d) represents a 4-cell dual-cleavage embryo; PPC-SR-μT external view from micromere dual (a) and from opposite macromere dual (b), and successive digital sections deep from macromere dual displaying

well-preserved yolk platelets. (e–h) a 32-cell embryo with a giant D quadrant showing PPC-SR-μT external (e) and transparent view (f) of a giant polar macromere, and from opposite micromere cap (g), an internal digital section slicing through the micromere cap. Scale bars = 400 μm (a–d) and 300 μm (e–h)

bilateral symmetry. It is promoted by either an inductive mechanism or cytoplasmic determinants, associated with the equal and unequal cleavage modes, respectively. The inductive mechanism represents the ground state of the quartet cleavage mode, characteristic of morphologically equal cleavage. The cytoplasmic determinants that act in the unequal cleavage mode cause an asymmetric distribution of the cytoplasm, creating one macromere (D cell) larger than the other three by either asymmetric cytokinesis or the formation of an enucleate membrane-bound protrusion (the polar lobe). The discovery of fossil quartet cleavage embryos with a giant D quadrant reported here (Fig. 14e–h; Chen et al. 2009b) suggests that the asymmetric cytokinesis underlying D-quadrant specification has an ancient Precambrian history. D-quadrant specification is critical in establishing the future axis of bilateral symmetry in the embryo, including many early key bilateral characters, in many lophotrochozoans and crustaceans. In addition to D-quadrant specification, the developmental sequences of early embryos, similar to the polar-lobe-forming embryos of modern spiralians (Chen et al. 2006), have also been recorded in the Weng’an fauna. As seen in some extant spiralian animals, polar lobe formation is one of the symmetry-breaking mechanisms that allow the partitioning of maternal cytoplasmic substances to certain blastomeres and not others. Polar lobe formation leads to unique early cleavage morphologies,

including trilobed, J-shaped, and five-lobed structures (Fig. 15). Thus, fossil embryos similar to modern lobeforming embryos are recognized from the Precambrian Doushantuo Formation phosphates, Weng’an, Guizhou Province, China. These embryos are abundant and form a developmental sequence comparable to the different developmental stages observed in lobe-forming embryos of extant spiralians. These data imply that lobe formation is an evolutionarily ancient process of embryonic specification and evolved before the Weng’an biota event (Chen et al. 2006). Xiao et al. (2007a, b) have recently reported finding fossil eggs with spirally decorated structures. These are interpreted as post-blastula-stage embryos. However, there is no internal structure and these forms could also be one-cell eggs according to the authors.

The Lower Cambrian Maotianshan Shale: A Unique Window on the Cambrian Explosion The biota of the Maotianshan Shale at Mt Maotian (Fig. 16) was first recognized for its excellent preservation with the 1984 discovery of naraoiids by X. G. Hou (Zhang and Hou 1985). Fossils from the Qiongzhusi Formation, cropping out widely in eastern Yunnan Province, were known and studied earlier in the twentieth century (e.g. Ho 1942) but the exquisite state of preservation of the fossils from the Maotianshan Shale

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Fig. 15 Polar lobe-forming embryos (a–l) from Precambrian Doushantuo Formation, Weng’an, Guizhou, in trefoil stage (a–g), J-shaped stage (h) and five-lobed embryos (i–l). Schematic diagrams (m–q) show changes in shape of the

PL-forming embryos in some extant molluscs and annelids— egg with the first lobe (m); trefoil stage (n); two-cell stage (o); J-shaped embryo (p); and five-lobed embryo (q). Scale bar = 250 mm

Fig. 16 Natural profiles of the lithologic sequence of the Early Cambrian at Mt Maotian, Chengjiang, Yunnan. The lithologic profile, photographed from the west, shows location of the

classic fossil quarry site and the Museum of Chengjiang Biota (adapted from Chen 2004)

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has resulted in it being intensively excavated and studied by many teams of researchers, yielding a constant flow of discoveries that has shed new light on the early evolutionary history of many animal groups and has also triggered extensive scientific debate around their interpretation. The profile of the Precambrian–Lower Cambrian rocks exposed at Mt Maotian and on its lower slope is shown as a continuous sequence (Fig. 17). It includes the following lithological units from oldest to youngest: Precambrian Baiyanshao Dolomite and Xiaowaitoushan Cherty Dolomite of the Dengyin Formation; Lower Cambrian Zhujiaqing Phosphate Formation and Lower Black Shale and Siltstone units of the Shiyantou Formation of the pre-trilobite deposits, and Upper Black Shale, Maotianshan Shale; and siltstone of the Yu’anshan Formation; and the overlying Canglanpu Formation. The Maotianshan Shale, 50 m thick at Mt Maotian, crops out broadly in east-central Yunnan (Fig. 18). Several tens of fossil localities have been excavated and are scattered throughout east-central Yunnan. Among these fossil localities, three sites are outstanding and have been extensively excavated and studied: Mt Maotian (Chengjiang), Haikou (Kunming), and Shankou (Anning) (Fig. 18). The fossil compositions at these three sites differ and are known as the Chengjiang, Haikou, and Anning fauna, respectively (Chen 2004). The Maotianshan Shale consists of fine mud deposits, excellent for the detection of sedimentary event layers (e.g. ash layers or tempestites). Each constituent event layer is 2–3 cm thick, displaying a graded unit at the base and an upper homogeneous fine mud unit. The upper unit is responsible for the exquisite state of fossil preservation. The taphonomy of these exceptionally wellpreserved fossils remains a mystery, although it had been discussed by several authors. They have proposed that storm-generating tempests (Zhang et al. 2009) or mud flows (Chen 2004) were responsible for the extraordinary preservation of the Maotianshan Shale faunas. However, these hypotheses do not accommodate the presence of mobile animals, especially the mobile mud burrowers (such as priapulid worms), active swimmers (early vertebrates, numerous arthropods, and anomalocarinids), and macroscopic pelagic animals (eldoniids, ctenophorans, vetulicolids, and some arthropods), because these animals could readily

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Fig. 17 Diagrammatic profiles of the lithologic sequence of the Early Cambrian in Mt Maotian area, Chengjiang, Yunnan (adapted from Chen 2004)

escape from such thin muddy event deposits. These event mud layers were thin (only 20 cm thick) even before dehydration.

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Fig. 18 Location of fossil sites of the Maotianshan Shale fauna

These thin mud layers are apparently insufficient for such excellent preservation. I suggest here that a poisonous event may have played a significant role, together with a sedimentary deposition event, in the exceptional state of the Maotianshan Shale preservation. These organisms may have been poisoned before they were buried by the event deposits. The Maotianshan Shale biota comprises an extremely diverse faunal assemblage, with more than 100 species described, displaying diverse body plans linked to those of many living phyla and subphyla. In animals, the body plan (or body form) is essentially the blueprint for the way the body of the organism is laid down (Raff 1996; Hall 1998). The blueprint is shared by a group of animals ranked together at a higher taxonomical level (phylum, subphylum, class, or order). It characterizes a unique anatomical body organization, is evolutionarily conserved, and is deeply rooted. The most interesting manifestations of the body plan in animals occur at the taxonomic level of the phylum and sometimes subphylum (especially in the Vertebrata). The Cambrian explosion was marked by many profound revolutionary changes and innovations,

including sudden increases in skeletization, numbers of species, complex ecosystems, intensive arms races, and body plans. Among these, the sudden increase in diverse body plans was the most remarkable, unique change. The Lower Cambrian Maotianshan Shale lies at the heart of the Cambrian explosion. The shale has preserved body plans of many bilaterian animal groups that are seen in living phyla, including chordates, ascidians, priapulids, sipunculans, arrow worms, possible molluscs, possible annelids, phoronida, and brachiopods (Chen 2004; Hou et al. 2004; Chen 2009) and at the level of the subphyla Vertebrata (Chen 2008) and Tunicata (Chen et al. 2003b). Many of these have changed very little since then (for instance, the ctenophores, priapulids, sipunculans, chaetognaths, tunicates, and inarticulate brachiopods). On the contrary, the animals with backbone are a magical and unique group of animals deeply rooted in the Early Cambrian. This is illustrated well by the outstanding ground body plan of the animals with backbones in the beautifully preserved fossils from the Lower Cambrian Maotianshan Shale. These shed light on the mysterious origins of many aspects of our own group, including

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the head, head sensorial organs, mouth, brain, pharyngeal system, and axial skeleton. Based on this ground plan, the animal group was subsequently upgraded, developing novel body plans at different evolutionary stages, represented by jawless fishes, jawed fishes, amphibians, reptiles, birds, and mammals, to create the wonderful pageant of evolution that has unfolded from the Cambrian to the present day. The limb-bearing segmented animals known as panarthropods have been diverse and abundant since the Early Cambrian and include diverse nested body plans representing different evolutionary stages. Unlike those of the crest animals, most of these different body plans appeared in the Early Cambrian. The successive emergence of these novel body plans near the root of the evolutionary history of the panarthropods is a remarkable phenomenon.

First Diversification of the Porifera The poriferans, or sponges, are a highly characteristic phylum of aquatic metazoans, typified by the presence of choanocytes, a system of branched canals with a collar chamber that transports water throughout the body. The adult has neither a mouth nor an anus. They are widely regarded as an isolated group among the animals. However, the sponges have some characters of intriguing evolutionary significance (Maldonado 2004), including their widely occurring internal fertilization, notable diversity of gastrulation modes, architecturally complex lecithotrophic larvae, their direct development in some groups, and the

Fig. 19 Panorama of diverse sponges in the Early Cambrian

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replacement of choanocyte-based filter feeding by carnivory in some sponges. Together these features strongly suggest that the sponges have a longer and more complicated evolutionary history than traditionally assumed and that the uncomplicated anatomy of modern adult sponges may be the result of secondary simplification. Adult sponges are uniquely specialized for filter feeding and their body is built according to one of three anatomical designs: asconoid, syconoid, or leuconoid. The asconoid type is the simplest, with the lowest filtering efficiency. The body is small and cylindrical, not exceeding a diameter of 1 mm and not much longer than 10 cm. The syconoid type displays clearly greater filtering efficiency than that of the asconoid sponges because the volume of the atrium is reduced and the area of the flagellated choanoderm is increased. Consequently, these sponges are generally larger with diameters ranging from one to a few centimetres. The body size of leuconoid sponges is the largest, ranging from a few centimetres to more than a metre. Sponges, widely recorded both in their adult form and as embryos in the Early Ediacaran Weng’an biota, have a deep Precambrian history (Li et al. 1998; Chen et al. 2009b) and diversify greatly until the Cambrian (Fig. 19). The sponges are the major components of the sessile colonies in the Maotianshan Shale fauna. About 30 species belonging to 20 genera have been recorded. Among these, the monaxonid demisponges predominate and are largely represented by complete or nearly complete skeletons. As epifaunal suspension feeders, they are adapted for muddy bottoms, with

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Fig. 20 Small sponges from the Early Cambrian Maotianshan Shale, central Yunnan. (a, b) photograph and restoration of Choia xiaolangtianensis; (c–f) photographs (c–e) and restoration

(f) of Crumillospongia sp. nov, and G, H, Saetaspongia densa. Scale bars = 0.5 cm (a, c–e), and 0.2 cm (g, h)

substrates varying from soft to semi-firm, and water energies ranging from extremely low to relatively high. The ecological tiering of the sponges in the Maotianshan Shale varies notably from those of only a few centimetres in some forms, such as Saetaspongia, Choia, and Crumillosponge (Fig. 20), to 30 cm in Quadrolaminiella (Fig. 21). The body diameter is only few millimetres in some species, whereas some species are much larger with diameters ranging from one to several centimetres. The largest, Quadrolaminiella, has a diameter of more than 10 cm and a length of 30 cm. There is no direct evidence of the design of their filtering chambers, but the size range of these fossil sponges indicates that all three anatomic designs for filter feeding observed in modern sponges had already evolved in Maotianshan times.

The small straw-hat-like sponge known as Choia was first recorded in the Middle Cambrian Burgess Shale. In the Maotianshan Shale, it is represented by the species Choia xiaolantianensis (Fig. 20a, b). The small disc-like body, about 1–2 cm in diameter, is composed of a single-layered skeleton consisting of a thatch formed by two sets of monaxial spicules, finer and coarser ones, extending radially from the centre of the body, reaching the body margin and far beyond the body margin, respectively. Choia is not common in the Maotianshan Shale. The small sac-like Crumillosponge is known from the Middle Cambrian Burgess Shale (Rigby 1986; Walcott 1919). It also appears in the Maotianshan Shale but is uncommon. Figure 20c–f shows new species of the genus from the Maotianshan Shale.

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Fig. 21 Elongate sponges from the Early Cambrian Maotianshan Shale, central Yunnan. (a–c) photographs (a, b) and restoration (c) of Leptomites teretiuslulus, showing doublelayered skeleton, with outer layer consisting of long, vertical spicules and inner layer composed of a thatch of tiny horizontally arranged spicules. (d) photograph of Leptomitella conica showing outer layer of skeleton consisting of a vertical thatch of fine

spicules and associated vertical rod and inner layer composed of both bundled and unbundled horizontally arranged spicules. (e, f) photograph (e) and restoration (f) of Paraleptomitella dictyodroma showing outer layer of skeleton consisting of coarse and curved monaxons and fine vertically arranged spicules, and inner layer formed by bundles of horizontally arranged spicules. Scale bar = 1 cm

The sac-like body is small, 10–15 mm in diameter, topped with a wide opening, the osculum. The osculum is clearly rimmed with small, densely packed spicules along its margin. The wall is perforated with

poles, interpreted as ostria, occurring as two differently sized sets: the larger is about 1 mm in diameter and smaller is only 0.3 mm in diameter. The tracts are composed of numerous, parallel, monaxon spicules;

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

these extend throughout the area between the ostria in various directions. As the base of the body is broadly rounded and there is no evidence of an attachment structure, it seems that the animal was not anchored to the substrate. The spherical sponge known as Saetaspongia densa (Mehl and Reitner in Steiner et al. 1993) is a monospecific genus, recorded only in the Maotianshan Shale (Fig. 20g, h). It is small, up to 3 cm in diameter, and the skeleton is mainly composed of monaxonic diactine spicules. In addition to the monaxonic spicules, there are small spicules in three-, four-, and even sixrayed forms. The flattened outline of the body probably represents an oscular opening. The presence of small polyrayed spicules suggests that the species belongs to the Hexactinellida, the glass sponges. No attachment structure has been found, suggesting that the animal rested on the substrate with the osculum opening upwards. Sponges with an elongated tube-like body form range in diameter from 0.6 to 2 cm and are about 10 cm in length. They are the dominant forms in the Maotianshan Shale including species of Leptomitus Walcott, 1886, Leptomitella Rigby, 1986, and Paraleptomitella Chen et al. (1989a) (Fig. 21). Their two-layered skeleton is formed by simple monaxial spicules, with a vertical thatch consisting of an outer layer of coarse spicules interspersed with densely packed fine spicules, and a horizontal thatch consisting of an inner layer of fine spicules. These fine spicules are evenly distributed in Leptomitus Walcott,

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1886 (Fig. 21a–c), but are arranged into bundles or are unbundled in Leptomitella Rigby (Fig. 21d–f). Unlike those of Leptomitus and Leptomitella, the outer layer of the skeleton in Paraleptomitella is formed of both curved coarse spicules and densely packed fine spicules. A vase-shaped sponge known as Quadrolaminiella Chen et al. (1990), is the largest of the Maotianshan sponges, with a diameter of 10–20 cm and a length of 30 cm (Fig. 22). It has a thick, four-layered skeleton composed of simple monaxial spicules. The vertical thatch in its outermost layer is composed of coarse and widely spaced spicules that extend vertically through the entire length of the body. The horizontal thatch inside the vertical thatch is formed by fine, dense, and densely packed spicules. The two inner layers are composed of widely spaced coarse spicules interspersed with fine spicules. The thatch of these two layers is composed of spicules that extend diagonally along the body axis but in opposite directions. A unnamed new species of Halichondrites Dawson (1889), from the Maotianshan Shale is similar in size to Quadrolaminiella (Fig. 23). Its skeleton is two layered and composed of simple monaxial spicules. The outer layer is a vertical thatch composed of vertically extended and densely packed fine spicules and widely spaced coarser prostalia, extending vertically along the body, although their upper parts extend outward, curving from the skeleton to form a bush-like structure. The inner layer is composed of horizontally extended fine spicules that form bundles.

Fig. 22 Photographs (a, b) and restoration (c) of a large ellipsoidal sponge Quadrolaminiella diagonalis with 4-layered skeleton from the Early Cambrian Maotianshan Shale, central Yunnan. Scale bars = 2 cm (a), 1 cm (b)

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Fig. 23 Restoration and photograph of a large cup-shaped sponge Halichondrite sp. nov. from the Early Cambrian Maotianshan Shale, central Yunnan, showing a cup-shaped body with 2-layered skeleton; outer layer consists of axially arranged fine spicules; inner layer formed by bundled horizontally arranged spicules. Coarser spicules (prostalia) are axially extended and protrude radially from the body wall. Scale bar = 1 cm

Fossil Representatives of the Cnidaria

Chancelloriids and Possible Affinities

Representatives of the phylum Cnidaria, although not common in the Maotianshan Shale, include a few sea anemones and some other sessile polyps. The sea anemones are represented by Xianguagia sinica Chen and Erdtmann (1991); it is entirely soft-bodied and cylindrical in shape. Specimens are commonly preserved in a laterally compacted manner but a few have undergone oral/aboral compaction (Fig. 24). The diameter of the species is up to 3 cm, and the length is up of 6 cm. It consists of a smooth-surfaced pedal disc and a column with external stripe-like vertical structures. The outer surface of the column is ornamented with small knolls arranged linearly and vertically, with two lines in each strip. Sixteen flexible tentacles extend from the oral margin of the column and distally taper to a point. Archotuba Hou et al. (1999) is a tube dweller (Fig. 25). The tube is open at the wider end and usually attached to a brachiopod shell at the narrow end. The tube usually shows the presence of a funnel-like soft tissue. The closely related species Cambrorhytium Conway Morris and Robison (1988) from the Middle Cambrian, is preserved with tentacles on the distal end of the tube and is interpreted as a cnidarian.

Chancelloriids were a common element in the Cambrian small shelly fossil assemblages and extinct, star-shaped, Cambrian organisms, with hollow, spinelike sclerites. Well-preserved articulated exoskeletons (known as scleritones) are not common and are predominantly restricted to the Lower Maotianshan Shale and the Middle Cambrian Burgess Shale. Chancelloriids have been reconstructed (Janussen et al. 2002; Chen 2004; Randell et al. 2005) as sac-shaped, sessile, benthic animals covered in rows of spiny sclerites. The sclerites protrude from beneath an epidermal layer (Janussen et al. 2002; Chen 2004). The chancelloriids in the Maotianshan Shale are one of the most important elements among the sessile benthic fauna and are mainly represented by Allonina phrixothrix Bengtson and Hou (= Allonia junyuan Janussen et al. 2002). The body is sac-like (Fig. 26) and radially symmetrical, narrowing proximally and distally, and is covered with a continuous pliant integument, embedded with regularly disposed hard, mineralized composite spine-like sclerites (Fig. 27). The sclerites usually have three rays, with two rays buried in the integument (Fig. 27c, d), and these two rays form a V shape, with the open side directed distally (Fig. 27a). The other ray protrudes nearly vertically

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Fig. 24 Sea anemone Xianguanqia sinica from the Early Cambrian Maotianshan Shale, central Yunnan. (a, b) part and counterpart of a top-laterally compacted specimen showing: fully exposed tenctacles (a) and a body column (b). (c, d)

laterally compacted specimens showing a smoothly pedal disc, a column with external strip-like longitudinal structures with entire number of 16, each strip-like structure related to a tentacle. (e) restoration. Scale bar = 1 cm

from the surface in most parts of the body, except the distal part (Fig. 26). The angle between these external rays and the body axis tends to narrow. At the distal margin of the body, the rays protrude beyond the distal opening, extending either convergently or parallel to the body axis (Fig. 27a). The inter-sclerite integument has a conspicuous rhombic feature over the entire body (Fig. 27d–f). These rhombic structures are interpreted as the impressions of small, hard, embedded platelets (about 50– 60 μm long and 30–40 μm wide; Bengtson and Hou 2001). Bengtson and Hou (2001) observed the platelets to be thicker at the margin and depressed centrally, with a fine rod protruding from the surface.

Affinities The taxonomic affinities of the chancelloriids are uncertain. They were first described as sponges (Walcott 1920); the sponge hypothesis was challenged with the realization of their complex nature (Bengtson and Missarzhevsky 1981). Further research showed that the “spines” themselves were formed as dermal sclerites, rather than as spicules. In recent studies, the chancelloriids have been compared with either ascidians (Mehl 1996) or cnidarians (Chen 2004; Randell et al. 2005). The ascidian interpretation is based on a comparative study of spicules of the two groups

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Fig. 25 Photographs (a–d) and restoration (e) of tube dweller Archotuba of possible cnidarian affinities from the Early Cambrian Maotianshan Shale, central Yunnan, showing elongate

cone-shaped tube with proximal end attached to brachiopod shell and a distinct elongate cone-shaped organic structure within the tube (a–d). Scale bar = 0.5 cm

but as the study was based on evidence from photographs rather than on real specimens and absence of significant ascidian characters, including a branchial cavity or coiled intestine, it challenges this hypothesis.

Sclerite-based comparative analyses with ascidians (Mehl 1996) and octocorals (Randell et al. 2005) have provided limited support for the chancelloriid affinities. As observed in Allonia phrixothrix, the body

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embedded rays in each sclerite appears to vary. All these characters suggest that the radial rays of the sclerites were moveable, with a role in the contraction or expansion of the body.

Fossil Ctenophora Represents Evolutionary Transition to the Bilateria

Fig. 26 Laterally compacted Allonia phrixothrix from the Early Cambrian Maotianshan Shale, central Yunnan, showing two embedded rays divergin distally and a free ray protruding from body wall nearly vertically. Scale bar = 1 cm

in the chancelloriids is characterized by radial symmetry and a central cavity with a single distal opening, similar to the coelenteron in the cnidarians, and implying cnidarian affinities. The absence of tentacles suggests that chancelloriids were a very unusual animal group but related to the cnidarians. How they fed without tentacles remains unclear although some authors have proposed that the animals were filter feeders, with an inferred apical opening, and that the sclerites acted in a largely defensive role (Janussen et al. 2002; Randell et al. 2005). Our observations show that the pliant continuous integument was elastic and contractile. The chancelloriids may have fed from circulating water by drawing food-laden water into the coelenteron, with the waste water subsequently expelled from the coelenteron as the body repeatedly expanded and contracted. The external rays of the sclerites at the mouth margin extend either convergently (Fig. 27a, b) or vertically parallel to each other. The divergent angle of the two

The phylum Ctenophora (also referred to as “the comb jellies”), with 80 living species, are predominantly voracious gelatinous, planktonic, spheroidal to oblate predators. Although the phylogeny of the Ctenophora is inconclusive, they have traditionally been interpreted as a sister group of the cnidarians. The presence of mesodermal cells in the mesogloea, muscles in the tentacles, and acrosome-bearing sperm suggest that ctenophores are evolutionarily more advanced than the cnidarians and closely related to the bilaterians (Nielsen 2001). Since the Cambrian, ctenophorans have been predominantly marine dwellers and are an animal group with a few and morphologically conservative members. Exception to this conservative state are those species in the Middle Cambrian with more than 16 or 24 comb rows (Conway Morris and Collins 1996) and some rather bizarre body forms among modern species (Brusca and Brusca 1990). The body plan, as exemplified by a late-developing embryo (Fig. 28) from a phosphate bed at the base of the Lower Cambrian (Chen et al. 2007b) and adult forms from Maotianshan Shale deposits (Chen and Zhou 1997; Chen 2004; Figs. 29 and 30), is almost identical to the body plan of extant ctenophores, characterized by a spheroidal body with eight comb rows. Like some extant ctenophores, the mouth of the adult is surrounded by a broad skirt-like structure known as the “oral lobe”. The earliest firm evidence of the Ctenophora is an embryo from the Early Cambrian Meishucun phosphate deposit (Fig. 28) (Chen et al. 2007b). The 540-million-old embryo was preserved in a 10-cmthick bed of black bituminous phosphatic limestone near the base of the Kuanchuanpu Formation, overlying limestones containing the terminal Precambrian diagnostic fossil Cloudina. It was pre-mineralized by apatite of the kerogen, is about 190 μm in diameter with an enclosed embryo (≈ 150 μm in diameter) representing a late developmental stage before

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Fig. 27 Distal part of Allonia phrixothrix (a) and enlargements of the distal margin (b) and the integuments (c–f) in the distal part of the body, showing the external rays in distal margin extend either convergently or parallel to the body axis and

protrude beyond the distal margin (a, b); two internal rays in each sclerite were embedded in the integument; it displays a conspicuous rhombic texture (c–f). Scale bars = 1 cm (a), 0.5 cm (b, c, e), 0.1 cm (d, f)

hatching. The embryo is spheroidal and lacks tentacles, resembling in numerous respects the 10-millionyear-younger ctenophore Maotianoascus octonarius from the Maotianshan shale. Its aboral pole is represented by an incompletely formed apical (aboral) organ. The comb plates are represented in the embryo by meridional rows, each composed of a narrow striplike structure that corresponds to the combs of adult ctenophores. Like the comb plates of the larvae and

juveniles of modern ctenophores, these meridional rows originate from the apical organ and are attached to the epidermis of the specimen at its aboral end. The fluid-filled, branching, tubular meridional canals in living ctenophores underlying the comb plates are represented in the fossil by branching tubes filled with secondarily emplaced calcite. A complete array of eight comb rows is preserved in the embryo. The total number of comb rows appears to be the same

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

Fig. 28 Optical (a), Raman (b–f) and Confocal laser scanning microscopy (CLSM) (g, h) images of a thin section-embedded ctenophore embryo from the Early Cambrian Kuanchuanpu Formation of Ningqiang, Shaanxi. Blue in the Raman images displays the spatial distribution of carbonaceous kerogen; green

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is calcite; and red is apatite. Abbreviations: AO, apical (aboral) organ; EM, egg membrane; CT, ctenes; AC, aboral canal; MC, meridional. Scale bar in E = 25 μm (a, b, g); in E it represents 10 μm (c–f, g) (modified from Chen et al. 2007b)

Fig. 29 Restoration of Early Cambrian Maotianoascus octonarius

as in the Maotianshan Shale taxon and most modern ctenophores. The individual comb plates (ctenes) are 15–20 μm long and about 1 μm wide. The associated structures, originally hollow and fluid filled (e.g. meridional canals), and the interstices between them, are in-filled with calcite.

Digestion is extracellular in modern ctenophores, occurring in the pharynx, where ingested material passes into a complex system of radiating vascular structures that include the eight meridional canals, one beneath each comb row. The meridional canals in some ctenophores are branched. Composite images

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Fig. 30 Photographs of two laterally compacted specimens of Maotianoascus octonarius from the Early Cambrian Maotianshan Shale, central Yunnan; it shows a conspicuous aboral organ at the aboral pole; a stomadaeum enlarged in its oral portion with a large mouth; eight rows of ctenes extending from the aboral organ but ending at body constriction before reaching the mouth margin, a meridional canal lies beneath each of the comb rows and extends orally beyond the oral end of the comb row. Scale bar = 1 cm

produced with confocal laser scanning microscopy have documented the presence of eight such branched tube-like structures in the embryo studied here. The central part of the aboral hemisphere in modern ctenophores usually has a tube-like aboral canal (roughly comparable to the distal part of an intestine), a structure represented in the fossil by an unbranched elongate rod, ≈ 6.5 μm in diameter that extends orally from the apical organ for a distance of 40 μm to where it is buried beneath the branched canals of the comb rows. Living cydippids are widely accepted as representatives of the ancestral form of the Ctenophora. This implies that the ancestor of the ctenophorans had a spheroidal body form, eight comb rows, and a pair of tentacles. The cydippid hypothesis is challenged by the fossil evidence. Both the ancient 540-million-yearold ctenophore embryo and the 530-million-year-old adult M. octonarius from the Maotianshan Shale differ from living cydippids in being atentaculate and having branched meridional canals (Figs. 28, 29, and 30). Instead, these characters are shared by the embryos of extant beroidian ctenophores, to which this fossil seems more closely related. Furthermore, its apical organ is well developed like that of the embryos of most beroidians, although its domed form resembles that of the apical organ of some cydippids. On the basis of the characters exhibited by these embryo and adult fossils, the ancestor of the phylum was

an atentaculate, spheroidal organism, most closely allied to extant beroidians; it had a contractile oral lobe and used its comb rows for locomotion. The pelagic habit of the beroidians and most other modern ctenophores suggests that the common ancestor was also pelagic. In contrast with the pelagic interpretation, Shu et al. recently proposed that the early evolution of the ctenophores was marked by a shift from a benthic, sessile existence to a pelagic habit, coupled to a change in the function of their cilia from feeding to locomotion. Such a shift would involve major changes in their basic morphology and ecology and would require many (undocumented) intermediate stages. Based on this hypothesis, Shu et al. (2006) proposed the benthic, frondose Stromaveris psygmoglena from the Maotianshan Shale as a stemgroup ctenophore. This interpretation is based heavily on the presence of closely spaced branches, inferred to represent precursors of the diagnostic comb rows of ctenophores because they were “probably ciliated”. Cilia occur widely in both metazoans and protists, and they have diverse functions, not just in locomotion and feeding. Recourse to the presence of probable cilia as the prime character with which to infer a ctenophore affinity for S. psygmoglena is unconvincing. Similarly, the suggestion by Shu et al. that the Ctenophora occupies an intermediate evolutionary position between the sponges and cnidarians is inconsistent with numerous lines of evidence, both anatomical and molecular.

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Fig. 31 Panorama of diverse introvert-bearing worms in the Early Cambrian Maotianshan Shale: Maotianshania (1), Circocosmia (2), Palaeoscolex (3), Paraselkirkia (4), Corynetis (5), Anningvermis (6), Xiaoheiqingella (7), Acosmia (9), and Sicyophorus (10)

Three species of ctenophorans belonging to three different genera have been found from the Lower Cambrian Maotianshan Shale. They are Maotianoascus octonarious (Chen and Zhou 1997), Sinoascus palilatus (Chen and Zhou 1997), and an unnamed new genus and species. M. octonarious has a thimble-shaped ovoid body, about 3 cm wide and 4.5 cm long, arranged radially along the oral–aboral axis (Figs. 29 and 30). The oral portion of the stomodeum is enlarged, with a large mouth opening at the oral end. Its aboral side is regularly rounded with a conspicuous aboral organ at the aboral end. Between the two poles are eight well-developed rows of ctenes, originating from the aboral organ but end at the body constriction, long before reaching the mouth margin. Beneath each of the eight comb rows is a meridional canal. The meridional canals extend orally beyond the oral margin of the comb rows, presumably to join a circum-oral canal. Unfortunately, the circum-oral canal is not preserved in our specimen. S. palilatus is represented by a single specimen characterized by an ovoid body (1.3 cm wide and 2 cm long), possibly radially symmetrical along the oral– aboral axis. Between the two poles are four rows of possible ctenes. The aboral extremity has a depression surrounded by papillae, in which the statocyst was probably located.

Introvert-Bearing Worm-Like Organisms Introvert-bearing organisms are important members of the benthic communities, especially the endobenthic communities, in the Lower Cambrian Maotianshan Shale fauna (Chen 2004; Huang et al. 2004a, b;

Maas et al. 2007a, b; Dornbos and Chen 2008) and the Middle Cambrian Burgess Shale fauna (Conway Morris 1977a, 1993), occurring as at least 11 species in the Maotianshan Shale (Huang 2006) and 3 species in the Burgess Shale (Conway Morris 1979; Fig. 31). These Cambrian introvert-bearing organisms have been compared with living Priapulida. Their body forms include an elongated sac-like form, a slender vermiform, a loricated form, a dumb-bell-shaped form, and a tubiform, but except for Acosmia maotiania, these differ significantly from the body forms of living priapulids. The body of A. maotiania (Chen and Zhou 1997; Chen 2004) is elongate and sac like, resembling those of recent priapulids, especially Priapulus caudatus (Maas et al. 2007a, b) (Fig. 32). Whether all these introvert-bearing organisms from the Maotianshan Shale are priapulids remains an open question. Priapulida is a small phylum, with only 18 living species of marine worms. The phylum is a member of the cycloneuralians and is grouped with another four cycloneuralian phyla (Nematoda, Nematomorpha, Kinorhyncha, and Loricifera) to form the monophyletic taxon known as the “Introverta”, characterized by introverts and ecdysis. The priapulids are closely related to the kinorhynchs and loriciferans, with which they constitute the Cephalorhyncha, with several apomorphic features, including chitinous scalids on the introvert and two rings of pharyngeal retractor muscles penetrating the brain. Priapulids differ from kinorhynchs and loriciferans in that their introvert has an inversible mouth cone. The terminal mouth in priapulids is located at the anterior end of the resting introvert and opens into a muscular cuticularized pharynx lined with strong cuticle teeth. During feeding, it can

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Fig. 32 Extant priapulid: Priapulus caudatus (a), restoration (b) and photographs (c, d) of Early Cambrian Acosmia maotiannia. Scale bar = 1 cm

be everted (turned inside out) through the mouth, forming the mouth cone. The introvert-bearing worms from the Lower Cambrian Maotianshan Shale probably all had the inversible mouth cone typical of priapulids, although they were superficially significantly different from living priapulids. They may represent the stem lineage of the cephalorhynchs. Loricated forms, including Palaeopriapulites parvus (Hou et al. 1999; Chen 2004) and Sicyophorus

rara (Luo et al. 1999; Hou et al. 1999; Huang et al. 2004c; Chen 2004), from the Lower Cambrian Maotianshan Shale retain a body form resembling that of priapulid larvae, with a thick cuticular lorica (Fig. 33). These loricated forms have been interpreted as either Priapulida by some authors (Hou et al. 1999, 2004; Chen 2004) or Loricifera (Huang 2005). Although these Cambrian forms resemble modern Loricifera in having a life-time cuticular lorica, they

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Fig. 33 Loricated introvert-bearing worms from the Early Cambrian Maotianshan Shale. (a) a laterally compacted Palaeopriapulites parvus showing a bipartite body (introvert and trunk), an introvert bearing 20 rows of spines (larger anteriorly), trunk retaining 10 visible ridges; these suggest the total number of plates was 20 with an identical number of rows of spines which are smaller than those on introvert; intestine

simple, straight. (b, c) laterally compacted Sicyophorus rara showing bipartite body with introvert with 20 rows of spines arranged into an alternative order in 14 circles, a conical mouth cone lying front of the introvert; trunk bearing 10 visible plates (total number 20) and a large, tightly coiled gut within the lorica. Scale bar = 0.2 cm

differ from Loricifera in having a different number of plates, a much larger body (10–50 times larger), and in particular an inversible mouth cone. These dumbbell-shaped species display a striking resemblance to the loricate larvae of extant priapulids, particularly Tubiluchus corallicola (Van der Land 1968), with which they share identical numbers of loricate plates. The trunk of the loricate larva of Tubiluchus has ten ridges and ten depressions. Living priapulids have a biphasic life cycle and the lorica is only present in the larva, disappearing at metamorphosis. These fossils represent an instance of paedomorphosis, with the larval character retained in the adult. P. parvus (Hou et al. 1999; Chen 2004) is dumbbell shaped, with a size range of 3–5 mm (maximally 1 cm). The body is bipartite, separated into the introvert and the trunk. Both are an elongated ovoid shape; the introvert is slightly longer than the trunk bearing about 20 rows of spines increasing in height anteriorly. The trunk cuticle has ten visible longitudinal ridges, suggesting that it had 20 plates in total. The 20 rows of spines on the introvert are much smaller than those

on the introvert. The intestine is simple and straight, extending throughout the body (Fig. 33a). S. rara Luo and Hu (in Luo et al. 1999) (= Protopriapulites haikouensis Hou et al. 1999) occurs abundantly in Haikou and Anning, although Luo and Hu considered it rare (Fig. 34). The pharynx is elongated when it is protruded and is armed with tooth- or spine-like outgrowths, arranged in rows and circles, and occurring alternately between adjacent rings. The pharynx is possibly protrusive and retractable, and it bears regularly arranged spines, possibly in rings of five. The introvert has about 20 rows of spines, arranged into an alternative order in 14 circles. The conical structure lying in front of the introvert is the mouth cone, and its surface is smooth. The trunk cuticle is stiff and made up of longitudinal plates, the margins of which are visible as dark ridges. Ten ridges can be seen on one side, so overall there are 20 ridges. It has a large coiled gut within the lorica, making the retraction of the introvert difficult. This is a unique character unknown in other introvert-bearing organisms. P. parvus differs from S. rara in having a simple

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Fig. 34 Restoration of loricated introvert-bearing worm Sicyophorus rara

straight gut and a large introvert, slightly longer than the trunk. The loricate trunk is also present in the early larvae of living priapulids and throughout the lives of living loriciferans. It shares features with the early larvae of living priapulids in having the same number of plates (Lemburg 1999). The loricae of loriciferans all seem to be bilaterally symmetrical and consist of a greater number of plates. Yunnanpriapulus halteroformis (Huang et al. 2004c) and Xiaoheiqingella peculiaris Hu (Chen et al. 2002b) from the Lower Cambrian Maotianshan Shale have drum-stick (Figs. 35a and 36a, b) and dumb-bell forms (Figs. 35b and 36c), respectively. The scalid-bearing introverts of both are sub-spherical, with a corona. The anterior part of the introvert bears 25 rows of spines but the posterior part is smooth in X. peculiaris, whereas it has large, irregularly arranged spines in Y. halteroformis. The trunk is much longer than the introvert; it is elongated in X. peculiaris but has an expanded rear portion in Y. halteroformis. It is faintly annulated, and it is adorned with spines in the expanded rear portion in Y. halteroformis. The trunk bears a single, slender caudal appendage. The gut is preserved only in

Fig. 35 Restoration of introvert-bearing drum-stick-like worm Xiaoheiqingella peculiaris (a) and dumb-bell worm Yunnanpriapulus halteroformis (b)

Y. halteroformis, in which it is a large, locally twisted, tube-like structure. The slender introvert-bearing vermiform organisms in the Maotianshan Shale include Maotianshania (Figs. 37a and 38a, b), Cricocosmia (Figs. 37b and 38c, d), and Palaeoscolex (Figs. 37c and 38e–g). Maotianshania is known in Chengjiang, Cricocosmia occurs abundantly in both Haikou and Anning, and Palaeoscolex has a wide distribution in the Maotianshan Shale. All three taxa share characters, including an elongated and finely annulated trunk, an introvert, and a protrusile pharynx. They differ from each other by the smooth trunk in Maotianshania, the paired sclerites in Cricocosmia, and the densely arranged papillae in Palaeoscolex. Because of their superficial resemblance to nemathelminths, they have been interpreted as such by some authors (Hou and Bergström 1994; Hou et al. 1999, 2004; Maas et al. 2007a, b). However, the lack of the characteristic nematoid features in these

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Fig. 36 Introvert-bearing drum-stick-like worm Xiaoheiqingella peculiaris (a, b) and dumb-bell-like worm Yunnanpriapulus halteroformis (c) from the Early Cambrian Maotianshan Shale. Scale bar = 0.5 cm

Fig. 37 Restoration of slender introvert-bearing worms: Maotianshani cylindrica (a), Cricocosmia jinningensis (b) and Palaeoscolex sinesis (c)

Cambrian vermiform organisms makes the interpretation highly unlikely. The three vermiform organisms from the Maotianshan Shale all have a protrusile pharynx, an exclusively Priapulida character. The nemathelminths include the two living, possibly sister phyla, Nematomorpha and Nematoda. The nematomorphs are a small phylum containing free-living wormiform organisms with larvae that are exclusively parasitic on arthropods (Schmidt-Rhaesa 1996, 1997). They have no introvert and their gut is greatly reduced. However, the larvae bear 2–3 circles of six hooks, possibly homologues of the scalids of Kinorhyncha,

Priapulida, and Loricifera (Adrianov and Malakhov 1995; Malakhov and Adrianov 1995; Adrianov et al. 1998). The cuticle in the pharyngeal region is smooth, and chitin is absent in the adult but present in the larva. There are more than 20,000 species of nematodes, constituting more than 90% of recent nemathelminth species. The nematode body is cylindrical and tapered at both ends, and predominantly lacks an introvert. Thus, the considerable differences between them and the nemathelminths refute the interpretation that these Cambrian vermiform worms are nemathelminths.

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Fig. 38 Slender introvert-bearing worm Maotianshani cylindrica (a, b), Cricocosmia jinningensis (c, d) and Palaeoscolex sinesis (e–g) from Early Cambrian Maotianshan Shale. Scale bars = 0.5 cm (a–c, e, g); 0.2 cm (d); 1 cm (f)

Maotianshania (Sun and Hou 1987) lived strictly in the Chengjiang area and was apparently adapted as a burrower in soft, wet, muddy bottoms (Figs. 37a and 38a, b). The animals represent a pioneer species and constitute a predominant element in the area, living congregated in the mud layer. The animals are small (3 mm wide and 5 cm long), with a finely annulated trunk (3–4 annulations per millimetre). The gut has a simple tube form with annulations at its rear end and a pair of hooks on the rear surface. The spacing of the gut annulations appears to be identical to that on the body wall, suggesting the trunk annulations are not surface structures.

Cricocosmia jinniense (Hou and Sun 1988; Chen 2004; Maas et al. 2007a, b) occurs abundantly at both Haikou and Shankou, but rarely in Chengjiang (Figs. 37b and 38c, d). It was probably adapted to an epibenthic lifestyle. The animals are elongated (up to 10 cm) and are many times longer than their diameter (average diameter 0.25 mm). They lived in congregations. The inverted introvert is vase-like, with scalids arranged into circles, with the two distal circles larger than the other circles. The pharynx is long, with wider anterior and posterior portions and a constricted mid portion. The trunk is finely annulated, with 120 sclerite pairs. Each trunk annulation carries a pair of sclerites

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

ventrolaterally, except in the anterior part of the trunk. The sclerites are triangular with the narrow part anterior. The ventrolaterally situated sclerites might have facilitated an active type of locomotion on a semi-firm muddy seafloor. Palaeoscolex (Figs. 37c and 38e–g) is a wideranging form from Early Cambrian to Late Silurian strata. In the Maotianshan Shale, it is represented by Palaeoscolex sinensis (Hou and Sun 1988); it occurs at numerous localities in the areas of Chengjiang, Jinning, Haikou, and Anning. It has a diameter of 0.5 cm and its length exceeds 10 cm. The trunk is finely annulated, with five annulations per millimetre. The papillae are arranged transversely in lines, with two lines in each annulation. The everted introvert had a conic form. The pharynx has a mid constriction, as seen in Cricocosmia. Palaeoscolex Whittard (1953) has been assigned to, for example, the Annelida (Whittard 1953), Nematomorpha (Hou and Bergström 1994; Hou et al. 2004), and Priapulida (Chen and Zhou 1997; Conway Morris 1997; Chen 2004; Huang 2005). Isolated palaeoscolecidan annular plates have been widely recorded among small shelly fossils from different areas of the world (e.g. Hinz et al. 1990; Ivantsov and Wrona 2004). Forms of Pirapulida are characterized by their saclike body types and are represented by Corynetis brevis Luo and Hu (Luo et al. 1999) (Fig. 39a) and Anningvermis multispinosa (Huang et al. 2004b, c; Chen 2004) (Fig. 39b). The scalid-bearing introvert in the sac-like form is not well developed. It has a distinct corona, and the protrusile pharynx is highly developed. The trunk is undivided and adorned with papillae/spines that are arranged regularly to irregularly around the trunk. The trunk has an eversible caudal appendage. The gut is a simple tube. C. brevis is an uncommon species known only in Haikou and Shakou, and it is about 2 cm long (Fig. 40a–c). Its body is elongated and sac-like, divided into the introvert, trunk, and eversible caudal appendage. The introvert is smooth, except for its anterior termination, which bears a ring of coronal scalids. The protrusile pharynx is long and highly developed. The trunk has an extended rear portion, bearing faint but visible annulations and spines; these are long in the anterior part, short in middle part, and long and slender in rear part. A. multispinosa is 6 cm long, with an introvert similar to that of C. brevis (Fig. 40d, e). The pharynx is highly developed. The trunk is elongated, with closely arranged

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Fig. 39 Restoration of sac-like introvert-bearing worms Corynetis brevis (a) and Anningvermis multispinosa (b)

annulations, and is adorned with spines, tilted anteriorly, and becoming larger posteriorly. It has a long and slender caudal appendage and a simple, straight gut. A sessile priapulid-like animal known as Selkirkia sinica Luo et al. (1999) (= Paraselkirkia jinningensis Hou et al. 1999) from the Maotianshan Shale has been recorded in abundance in Shankou Haikou (Fig. 41) and was believed to have lived in colonies in firm muddy substrates (Fig. 42). The closely related species known as Selkirkia columbia Conway Morris 1977 was first recorded in the Middle Cambrian Burgess Shale. The Chinese specimens are treated as priapulids by several authors (Conway Morris 1977a, c; Hou et al. 1999, 2004; Chen 2004; Huang 2005); they are characterized as having an introvert region and an elongated, conically tapering trunk. Their introvert is distinctly separate from the trunk, has no annulations, and bears scalids in rows and circles, arranged alternately. A corona is present, but it is not as clear as in other forms. The pharynx seems to be protrusive and retractable, and bears spines arranged in circles and rows. The trunk is stiff, and it is presumed to be enclosed in a secreted tube by Hou et al. (1999, 2004). Alternatively, the tube may represent a firm cuticle (Mass et al. 2007).

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Fig. 40 Sac-like introvert-bearing worms Corynetis brevis (a–c) and Anningvermis multispinosa (d, e) from the Early Cambrian Maotianshan Shale. Scale bars = 0.2 cm (a), 0.5 cm (b–e)

Sipuncula

Fig. 41 Restoration (a) and photographs (b–c) of sessile introvert-bearing worm Selkirkia sinica from Early Cambrian Maotianshan Shale. Scale bar = 0.5 cm

Sipunculans (peanut worms) are a small phylum of non-segmented coelomate worms that live exclusively in a variety of marine habitats throughout the world (Cutler 1994). Although a number of species from different ages have been interpreted as sipunculans, the sipunculan identity of some of these species is highly questionable. These questionable species include Ottoia prolifica from the Middle Cambrian Burgess Shale (Walcott 1911a; Howell 1962), Lechaylus from the Silurian and Carboniferous (Weller 1925; Muir and Botting 2002), and Epitrachys rugosus from the Jurassic (Ehlers 1869). Some authors have proposed sipunculan affinities for hyolithids (Runnegar et al. 1975; Runnegar 1982). Like sipunculans, the extinct mollusc-like hyolithids had a convoluted U-shaped gut, with an anteriorly placed anus. However, hyolithids had a very unusual mineralized exoskeleton, consisting of a pointed shell with an operculum-like anterior lid, and some species had a pair of “helens”. These exoskeletal characters make a sipunculan affinity very unlikely. Three sipunculan worms have recently been recorded from the Lower Cambrian Maotianshan Shale: Archaeogolfingia caudata, Cambrosipunculus tentaculatus, and Cambrosipunculus sp. (Huang et al.

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Fig. 42 Sessile introvert-bearing worm Selkirkia sinica from Early Cambrian Maotianshan Shale, showing the organisms living colonially in firm mud bottom. Scale bar = 1 cm

Fig. 43 Photographs of extant sipunculan Phascolosoma granulatum (a) and Golfigia muricaudata (b) and restoration of Early Cambrian sipunculan Archaeogolfingia caudata (c) and

Cambrosipunculus tetaculatus (d) (a and b, courtesy of J Vannier and HY Huang)

2004a; Figs. 43c, d, 44a–c and d–f). Their sipunculan identities are attested by their • general morphology (“sausage”-shaped body with a slender retractable introvert and a wider trunk); • external features (e.g. perioral crown of tentacles, and hooks, papillae, and “wrinkled” rings on the body surface); and • internal features (U-shaped gut and an anus opening near the introvert–trunk junction). Among the sipunculan worms, A. caudata (Huang et al. 2004a), 4 cm long and 0.5 cm wide, is characterized by its relatively elongate introvert, which tapers forward (Figs. 43c and 44a–c). The trunk is as long as the introvert and bears fine ring-like wrinkles along its

mid and posterior parts. It terminates posteriorly in a cone-shaped end. The wrinkle pattern on A. caudata is similar to that of some living, contracted sipunculans. The trunk is covered with minute spot-like papillae, more densely distributed at the posterior end, as is also typical of many modern sipunculans. The trunk ends in a slender tapered projection, similar in shape to the caudal appendage of modern golfingiid sipunculans (e.g. Golfinigia muricaudata; Fig. 43b) (Saiz Salinas 1993; Cutler 1994). The digestive tract is U-shaped, recurving near the posterior end of the trunk. C. tentaculatus (Huang et al. 2004a) is 4 cm long and 0.4 cm wide and has an elongated body tapering anteriorly, with no clear boundary between the

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Fig. 44 Photographs of sipunculan Archaeogolfingia caudata (a–c) and Cambrosipunculus tetaculatus (d–f) from Early Cambrian Maotianshan Shale. Scale bar = 0.5 cm (a–d) and 0.2 cm (e, f)

introvert and trunk (Figs. 43d and 44d–f). As in most extant forms, the introvert is armed with anterior hooks that are larger at the anterior ring and smaller posteriorly. The introvert is tipped with a crown of small peripheral tentacles. The crown of tentacles is usually inverted and invisible in most specimens. The trunk is longer than the introvert, with a rounded posterior end, and is decorated with fine papillae. The digestive tract is U-shaped, recurving near the posterior end of the trunk. Both the descending and ascending portions of the tract are quite straight and close to each other. The digestive tract terminates in a circle-like structure representing the anus. C. tentaculatus shows a strong similarity to the living sipuncular Phascolosoma (Fig. 43a). These sipuncular fossil forms from the Lower Cambrian Maotianshan Shale display striking similarities to extant sipunculans, especially Golfidiidae. This implies that the sipunculans are not only deeply rooted in the Early Cambrian but have evolved very little since the Early Cambrian.

Worm-Like Organisms with Possible Polychaete Affinities The evidence of annelids in the Maotianshan Shale is relatively flimsy but the two species collected, Facivermis yunnanicus (Hou and Chen 1989) and

Maotianchaeta fuxianella (Chen 2004), are possibly related to extant polychaetes. F. yunnanicus is one of the Cambrian mysteries, with great controversy surrounding its affinities (Figs. 45 and 46). The wormiform organism (6 cm long) has a bipartite body, an anterior appendage-carrying head, and a trunk. The head has a small, short, conic non-segmented part and five segmented parts, each bearing a pair of head appendages protruding ventrolaterally. The anterior non-segmented part bears a terminal mouth. Each appendage has two rows of longitudinally aligned setae, the anterior and posterior rows. They are closely annulated, with 50–60 annulations per centimetre, each bearing a pair of setae, an anterior and a posterior one. The trunk is cylindrical for most of its length, with an expanded rear portion bearing 2–3 circles of small hooks. Parapodium-like structures are preserved, nearly 1 mm long, and extending lateroposteriorly. The gut is a simple tube-like structure with termini at both ends of the body. M. fuxianella (Chen 2004) is represented by a single, incompletely preserved specimen, about 5.4 cm long (incomplete length) and 0.6 cm wide, with pairs of laterally extended parapodia, which are elongated with distal setae (Fig. 47). Pairs of organic structures are situated at the lateral margin of the trunk, corresponding to the pairs of parapodia. These organic structures may represent the remains of the metanephridia.

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Fig. 45 Restoration of Facivermis yunnanicus

Although the annelids are broadly accepted as having an ancient origin, reliable polychaetes are first recorded in the Middle Cambrian Burgess Shale. Facivermis has a non-segmented acron and possible parapodia, displaying an affinity to the polychaetes. In addition to the acron, the head of Facivermis also includes a distinct five-segmented part, each segment bearing a pair of large appendages. A similar segmented head with paired appendage-like structures is also present in some living polychaetes, such as Odontosyllis enopla, found in shallow bays around Bermuda (Sterrer 1986). Maotianchaeta has been reported from the Maotianshan Shale and is similar to the polychaetes in having parapodia-like structures.

Soft-Bodied Mollusc: Vetustovermis There are 85,000 recognized extant species of molluscs, highly diverse in size, anatomical structure, behaviour, and habitat. There is good evidence for the appearance of shelled molluscs in the Early Cambrian and their diversification into gastropods, cephalopods, and bivalves in the Late Cambrian. However, the evolutionary history of both the molluscs’ emergence from the ancestral Lophotrochozoa and their diversification into the well-known living and fossil forms are still vigorously debated. Ancestral molluscs are widely accepted as having been shell-less, resembling modern aplacophorans, or

to have lacked continuous biomineralized exoskeletons, like extant chitons (Brusca and Brusca 2002). Radular grazing trace fossils (Radulichnus; Erwin and Davidson 2002; Seilacher 1999, 2003), together with large imprints of possible soft-bodied molluscs (Kimberella; Erwin and Davidson 2002; Fedonkin and Waggoner 1997; Seilacher 1999, 2003) from the latest Neoproterozoic Ediacaran indicate that macroscopic soft-bodied molluscs may have a deep Precambrian evolutionary history. The preservation of early shellless molluscs may have been unlikely, and the recognition of these fossils difficult, and they have been recorded extremely rarely in the literature (Sutton et al. 2001). Radular grazing traces preserved together with circular impressions (about 10 cm) in Lower Cambrian strata suggest the presence of soft-bodied macroscopic molluscs in Cambrian times (Dornbos et al. 2004; Fig. 48). Although the Lower Cambrian Maotianshan Shale had the potential to preserve soft-bodied fauna, no softbodied molluscs have been recorded from it, perhaps because they are difficult to recognize. However, a possible example is Vetustovermis planus, first described as an annelid by Glaessner in 1979 and as an arthropod by Luo and Hu in 1999 (Luo et al. 1999). Its molluscan affinities have recently been recognized with the study of new fossil specimens (Chen et al. 2005). The animal V. planus is slug like, flattened dorsoventrally, and 5–6 cm long (maximally 10 cm).

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Fig. 46 Facivermis yunnanicus from Early Cambrian Maotianshan Shale. (a, b) part and counterpart of a dorsoventrally compacted specimen, showing: head tentacles, parapodia (marked with arrow) and simply straight gut; (c1-3) showing head tentacles (c1-2) with setae (c2), anterior

non-segmented part (acron) (c2) and parapodia (c3, marked with arrow); (d) showing head tentacles and gut; (e) a laterally compacted specimen, showing head tentacles and gut. Abreviations: g, gut; p, parapodia. Scale bars = 1 cm (a, b), 0.5 cm (c1, d), 0.2 cm (e)

The rounded head is small but distinct, carrying a pair of large cephalic tentacles projecting from the dorsal surface of its middle part (Figs. 49a, b) and a pair of large, stalked eyes near the base of the tentacles (Fig. 50a, b, d). The trunk is ovally elongated and broadly triangular anteriorly (Fig. 50a, b, d, g, h), and decorated

with hard, short, cone-shaped spicules on the dorsal surface (Fig. 50b, e, h). It is laterally finned and the fins were flexible, extending continuously along most of the trunk, except on its triangular anterior part. About 50 pairs of transversely extending barlike structures, interpreted as gills, dominate the trunk. The gill bars are usually black, suggesting that they

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Fig. 47 Maotianchaeta fuxiannella from Early Cambrian Maotianshan Shale. (a, b) part and counterpart of the holotype. Scale bar = 1 cm

are organic. These gills are separated into two lateral sets by a dorsal midline and the lateral margin of the bar series is slightly separated from the trunk

Fig. 48 Rounded impression with radular grazing trace from Early Cambrian phosphate deposits, Jinning, Yunnan. Scale bar = 10 cm

margin, as would be expected for gills. These gill bars are more-or-less straight, evenly spaced over the whole trunk (Fig. 50c), tilted anteriorly, and overlap one another as the result of dorsal compaction. The common occurrence of deformation indicates that they were soft and flexible. These soft and flexible transverse gill bars could be gut branches (“gut diverticula”), known in flatworms. However, unlike gut diverticula, these bars are widely separated from the gut (Fig. 50c). The trunk retains a muscular foot-like structure ventrally. The foot is large, extending to cover most of the ventral surface of the trunk proper except for the most lateral parts of the gill bars (Fig. 50b, g). The lateral margin of the foot is also visible in most specimens split along the dorsal surface, as a series of projections visible beyond the outer margin of the trunk proper. These relationships suggest that the foot was relatively thick.

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Fig. 49 Anatomical features of the Early Cambrian mollusclike organism Vetustovermis planus. (a) dorsal view; (b) reconstructed cross-section. Abbreviations: A, anus; B, buccal mass and stomach; D, diverticula; Da, dorsal aorta; E, eye; F, foot; Fn,

fin; G, gills; H, head; I, intestine; M, mantle; O, outer margin of foot; P, spine-like structure; T, cephalic tentacles (adapted from Huang et al. 2004a)

The ventral foot shows a striking resemblance to the ventral sole of some modern flatworms. In dorsal view, the gill bars are separated by an axial band-like gut (ca. 3 mm wide) into the right and left gill parts. V. planus has a complete gut. The head contains a bulb-like structure interpreted as a buccal/stomach mass (Fig. 50a, b). It is commonly preserved in three dimensions, with an expanded, ramified anterior part. The ramified structures are interpreted as gut diverticula. The intestine is represented by a wide, partially mud-filled, three-dimensional tube-like structure (ca. 0.5–1 mm in diameter) that extends axially within the trunk proper with an anal opening just in front of the end of the trunk. The slender dorsally situated, tubelike structure (ca. 0.2 mm in diameter) seen in several specimens is interpreted as a median dorsal aorta, as seen in extant polyplacophorans. The flattened body and horizontal fins of V. planus could be adaptations to support the animal as it moved on the soft seafloor and for gliding or swimming near the seafloor. The large surface area of the gills may have provided effective gas exchange for an active life style. The well-developed sense organs include a pair of large, stalked eyes, and large cephalic tentacles, suggesting that V. planus was attuned to the presence of food resources and possible predators.

V. planus (Fig. 49) resembles the molluscs in having a flat foot, a polyplacophoran-like flexible, elongated body, and serial pairs of gills on each side of the trunk (Brusca and Brusca 2002). The dorsal, conic spinelike structures could be homologous to the cuticular spicules of the polyplacophorans and aplacophorans. The variety of characters is not specific to any crown group of molluscs (Brusca and Brusca 2002). For instance, a well-differentiated head is considered to be an advanced character and is absent among the more primitive molluscs. The sluggish head of V. planus suggests that the head could have been well developed in the early active pelagic molluscans. The gills in Vetustovermis are also simply bar shaped and could represent a primitive form, differing from other molluscan gills. The stalked eyes and tentacles are also present in both arthropods and annelids, although those groups lack the ventral foot, instead using leg-like appendages for locomotion. One might argue that the axial band-like visceral cavity of V. planus is a notochord and that the transverse bars are not gills but myomeres, thereby implying that the animal is a chordate. However, no known chordate has stalked eyes or a ventral foot. V. planus resembles some planktonic nemertine worms, especially Nectonemertes and Balaenanemertes, in several respects (Gibson 1972; 

Fig. 50 (continued) centre—some of the gills are bent—the imprints of spine-like structures; and a median dorsal aorta. Scale bars are all 5 mm except for E, which is 1 mm. Abbreviations: A, anus; B, buccal mass and stomach; D,

diverticula; Da, dorsal aorta; E, eye; F, foot; Fn, fin; G, gills; H, head; I, intestine; M, mantle; O, outer margin of foot; P, spine-like structure; T, cephalic tentacles

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Fig. 50 Vetustovermis planus from Early Cambrian Maotianshan Shale. (a, b) part and counterpart of a nearly complete specimen showing a small round head (a) with a pair of cephalic tentacles (b) and stalked eyes (a and b), a buccal mass and stomach with anterior diverticula (a), as well as lateral margins of a large ventral foot lying near the outer margins of the trunk (b) and imprints of dorsal spine-like structures, dorsal artery, intestine and an anus; (c) trunk showing gills and a mud-filled intestine; (d) a sagittal plane near the dorsal surface

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showing cephalic tentacle, eye, lateral fins, and a dorsal artery; (e) enlargement of A showing conic (red arrow) and rounded (white arrow) imprints of spine-like structures. (f) head of an animal showing a round head, a three dimensionally preserved buccal mass and stomach with anterior diverticula; (g) a sagittal plane near the ventral surface of a trunk showing ventral foot with its outer margins and gills in lateral area of the trunk proper, intestine, and folded lateral fins; (h) a sagittal plane near dorsal surface of a trunk showing gills extended axially near the

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Hyman 1951). These include an anterior tentacle, lateral fins, ventral foot, and a series of internal gut caecae comparable to the “gills” of V. planus. However, nemertines lack a protective cuticle or exoskeleton, as well as stalked eyes, and have a characteristic eversible proboscis. The presence of spine-like protective structures and stalked eyes and the absence of a proboscis do not support a nemertine affinity for the animal. The ventral flat foot also represents a trait that is shared with many turbellarians (free-living flatworms; Hyman 1951; Ruppert et al. 2004). The combined existence of a head, elaborate paired tentacles, and stalked eyes gives no support to an affinity between this animal and the flatworms. Some polychaetes, such as the sea mouse (Aphrodite aculeate), also have a ventral muscular creeping sole, and myzostomids have a circular body with fused parapodia; these form a ventral foot-like structure. However, the sea mouse is covered with a thick felt-like or hair layer and myzostomids have numerous extended cirri (Rouse and Pleijel 2001; Ruppert et al. 2004). Vetustovermis possibly represents an extinct, stemlineage molluscan, with similarities to the shellless sea slugs (gastropods that evolved from shelled ancestors) (Yonge 1960). Similar sluggish animals have also been recorded from the Middle Cambrian Burgess Shale. They include Nectocaris (Conway Morris 1976), Amiskwia (Walcott 1911a), Odontogriphus (Conway Morris 1976), and Pikaia (Walcott 1911b). V. planus also resembles the problematic Carboniferous T. gregarium in several important respects (Foester 1979). These include a dorsoventrally flat trunk, lateral fins, distinct visceral mass, stalked eyes, and a series of transverse segments. Foester has tentatively interpreted T. gregarium as a prosobranch gastropod (Conway Morris 1976). Among them, Nectocaris resembles strikingly to Vetustovermis by sharing an open axial cavity with paired gills; wide lateral fins; a single pair of long, prehensile tentacles; and a pair of stalked eyes. Smith and Caron (2010) interprets these naked sluggish animals as stem-lineage cephalopods, although the first shelled cephalopods evolved in late Cambrian (Chen and Teichert 1983a, b).

Chaetognathids (Arrow Worms) Chaetognatha (arrow worms) is a minor phylum of pelagic marine animals, consisting of about 150 living species. They are found in oceans throughout

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the world and play an important role in the food web as primary predators. Their body form is reminiscent of an arrow, so they are usually referred to as “arrow worms”. However, the fossil record of the Chaetognatha is sparse and the Carboniferous Paucijaculum samamithion is the only definitive fossil chaetognath. Some Cambrian protoconodonts could represent the grasping spines of this group. The Middle Cambrian Amiskwia has been considered a chaetognath, but with a slug-like head, terminal anus, and cephalic tentacles, it could well be a molluscan. The body plan of the arrow worms is characterized by a small slender body with strikingly perfect bilateral symmetry. It is divided into a distinct head, finned cylindrical trunk, and a dorsoventrally flattened, finned post-anal tail. The head is ovoid, with a depression that leads to a ventral mouth. The vestibule is flanked laterally with grasping prey-seizing spines. Eognathacantha ercainella (Chen and Huang 2002) and Protosagitta spinosa Hu 2002 (Chen et al. 2002b) are fossil representatives of the first arrow worms from the Lower Cambrian Maotianshan Shale. E. ercainella is represented by a single specimen, about 25 mm long. The animal might have been relatively rigid. It consists of a head, a trunk, and a possible tail (Fig. 51). The rounded head is wider than long, measuring about 2.8 mm in width; it is also wider than

Fig. 51 Restoration of Early Cambrian arrow-worm Eognathacantha ercainella from Early Cambrian Maotianshan Shale

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Fig. 52 Arrow worm Eognathacantha ercainella from Early Cambrian Maotianshan Shale. (a, b) part and counterpart of nearly complete specimen. (c, d) enlargement of anterior portion of part and counterpart. Scale bars = 0.5 cm (a, b) and 0.1 cm (c, d)

the rest of the body. Projecting anteriorly and laterally from the head are about 12 slightly recurved grasping spines, each about 900 μm long (Figs. 51 and 52a, b). Like those of modern chaetognaths, the spines have an expanded base and were probably embedded within the tissue. In the anterior part of head, there are numerous smaller spine-like structures (about 200– 250 μm long), interpreted as possible teeth. In the middle part of the head, there are numerous blueish papillae-like structures (about 150 μm long) surrounding a small slit-like structure, interpreted as a possible mouth (Fig. 51). The pair of transverse, cup-like structures at the posterior margin of the head is interpreted as the muscle marks of a hood. Such a hood is diagnostic of chaetognaths, and it is an extension of the epidermis, attached ventrally between the head and the trunk. The hood has retractor and extensor muscles.

The thick, brown envelope over the head is presumably a cuticle, as in recent chaetognaths. The cuticle disappears at the border between the head and trunk. In contrast to the head, the trunk (2.5 mm wide and 15 mm long) lacks evidence of a cuticle. The trunk epiderm, light yellow in colour presumably has no cuticle. The posterior part of the body is about 8 mm long, with a thick brown envelope; this is considered to be a tapering tail. If the envelope represents a cuticle, it differs from the cuticle-less tails of most living chaetognaths. Modern chaetognaths usually have paired lateral fins and a wide tail fin, all of which are supported by rays. However, in E. ercainella, only a pair of narrow fins without fin rays is preserved. The fins extend continuously from the anterior part of the trunk, throughout the trunk and the tail. It is impossible to

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determine whether the fins are in the frontal plane of the body, as in modern chaetognaths, or otherwise disposed. The fins have a uniform width of 0.4 mm, except throughout the anterior 2 mm, where they narrow anteriorly. No widening of the tail fin can be seen in the fossil form. A bulbous structure at the anterior end of the trunk is presumably a pharynx (bulbate in modern chaetognaths) narrowing posteriorly to join a slender light-bluish line, interpreted as the intestine running posteriorly, with a possible anus at its posterior end in front of the tail. The position of the possible anus, just anterior to the tail, corresponds to that in extant chaetognaths. The affinity of E. ercainella with chaetognaths is supported by a widened head, distinct from the trunk, its presumed tail (based on the cuticularizaton in the fossil form), grasping spines and possible teeth on the head, and a hood at the border between the head and the trunk.

Limb-Bearing Creatures: Panarthropods Panarthropods, the first limb-bearing creatures, were diverse in the Early Cambrian. They are probably a monophyletic taxon, sharing a body pattern that includes several important characteristics: a segmented body, paired appendages, and a chitinous cuticle that is moulted during ecdysis (Ruppert et al. 2004). The presence of pyramid-yolk embryos (Chen et al. 2004d) and late-developing embryos with a segmented germ band (Chen 2004; Steiner et al. 2004) (Fig. 53) in the very basal parts of the Lower Cambrian Meishucun phosphate deposits suggests that the pararthropods are deeply rooted at the very beginning of the Cambrian, about 542 million years ago or even earlier. The exceptionally well-preserved fossil fauna from the 530million-year-old Maotianshan Shale deposits provides a fossil record of remarkably diverse panarthropods, with a number of body organizations representing different evolutionary stages (Fig. 54). These include the worm-like stem-lineage panarthropods, referred to as Tardiopolypoda (Chen and Zhou 1997), stem-lineage arthropods (proarthropods; Chen 2004; Waloszek et al. 2005), stem-lineage euarthropods, and the possible ancestral form of the two major extant euarthropod groups, the Chelicerata (Chen et al. 2004c) and Mandibulata (Chen et al. 2001). These nested body plans representing different evolutionary stages

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suggest the presence of step-wise and condensed evolutionary events in the evolutionary pathway from the worm-like ancestor to the euarthropods within a short geological period of about 12 million years in the Early Cambrian.

Worm-Like Stem-Lineage Panarthropods The Maotianshan Shale has produced Tardipolypoda (Chen and Zhou 1997), worm-like organisms with unjointed limbs. These are the least complex of the Panarthropoda and represent the stem-lineage panarthropods. The group is highly diverse and includes Luolishania longicruris (Hou and Chen 1989), Microdictyon sinicum (Chen et al. 1989a; Ramsköld and Chen 1998), Cardiodictyon catenulum (Hou et al. 1991), Onychodictyon ferox (Hou et al. 1991), Paucipoda inermis (Chen et al. 1995c), and Hallucigenia fortis (Hou and Bergström 1995; Ramsköld and Chen 1998). These taxa share several important characteristics: a soft, segmented body with paired appendages, an undifferentiated head that is either segmented or of non-segmental origin, and a mouth and anus at either end (Ramsköld and Chen 1998; Ramsköld 1992). An anatomical analysis of the tardipolypods testifies to the rapid evolution at the base of the Panarthropoda as they are separated by morphological gaps into several different groups based on their head plan: a non-segmental head, a one-segmented head, or a two-segmented head (Fig. 54). The non-segmented-head tardipolypods, including M. sinicum (Figs. 55 and 56) and P. inermis (Fig. 57), have the least complex head, relatively long in both M. sinicum and P. inermis, but differing morphologically, being cylindrical in P. inermis and narrowing anteriorly in M. sinicum. A morphological gap is also great in the trunk anatomy of these two species, in so far as they differ in their numbers of segments and their surface structures; the surface is nearly smooth in P. inermis but is adorned with a pair of structurally complex, hard, lateral sclerites on each trunk segment in M. sinicum. These sclerites, hard and possibly mineralized, occur widely among Lower and Middle Cambrian rocks. The generic name Microdictyon was erected to represent these remarkably complex sclerites by Bengtson, Matthews, and Missarzhevsky in 1981 (see Missarzhevsky and Mambetov 1981;

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Fig. 53 Yolk-pyramid eggs (a–e) and late developing embryos with segmented long germ band (f–h) from Early Cambrian Kuanchuanpu formation, Ningqiang, southern Shaanxi. Explanatory (a-0) and light transparent images of the eggs (a-1 and a-2) at early yolk-pyramid stage with about 120 yolkpyramids; Explanation (b-0) and light transparent images of

eggs (b-1 and b-2) are at late yolk-pyramid stage with about 360 yolk-pyramids. SEM images show the surface (c) and internal yolk-pyramid structures of eggs d–e and f–h; these are SEM images of late-developing eggs showing long segmented germ-band. Scale bar = 200 μm

Bengtson et al. 1986) based on sclerites recovered from rocks in the Atdabanian Stage, Siberia. These remarkable sclerites, with their striking resemblance to complex arthropod eyes, created great confusion before the first complete animal was recovered at 1989 in the

Maotianshan Shale and designated M. sinicum (Chen et al. 1989a). M. sinicum is a worm-like animal, with a maximum length of 9 cm (Figs. 55 and 56). The body is basically cylindrical in shape, except for the tapering head. The body of the animal is differentiated into two

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Fig. 54 Body organization in extinct stem lineages in Panarthropoda. (a) non-segmented head, exemplified by Microdictyon sinicum; (b) one-segmented head with a pair of head appendages, exemplified by Onychodictyon ferox; (c) two-segmented head with two pairs of head appendages, exemplified by Hallucidegia fortis (adapted from Chen 2009)

distinctly different parts, the head and the trunk. The region anterior to the first pair of sclerites represents the long head tapering about one-fifth the length of

Fig. 55 Restoration of Early Cambrian Microdictyon sinicum

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the body to a terminal mouth. The trunk is cylindrical and annulated, with a conspicuously rounded swelling, dorsal to the sclerites. It ends with a small protrusion referred to as the “anal protrusion”, with an anus opening at its terminus. The trunk is subdivided into eight subequal segments with nine pairs of sclerites, and is supported by 10 pairs of unjointed limbs. The sclerites vary in both size and morphology, with the anterior pair the smallest, and increasing in size posteriorly. The first pair is vertically elongate, pairs 2–8 are vertically oval with some being tear-drop in shape; the last pair have a sub-quadrant form. The sclerites are situated on the lateral trunk, dorsal to the limbs, and each corresponds to a limb, except for the last pair, which corresponds to two pairs of limbs. Limbs are tubular, marked with faint annulations and have two terminal claws. Bent claws are directed posteriorly, except those on the last pair of limbs, which are directed anteriorly. The first pair of limbs is longer and more slender than the remaining pairs of limbs, sub-equal in length. The centroventrally situated gut is a simple tube opening at both ends of the body. P. inermis (Fig. 57) has the least complex body form, shaped as a simple cylinder supported by six pairs of limbs. The claws are oriented as in M. sinicum. O. ferox (Figs. 58 and 59a, b) represents the group having a single, segmented head. The trunk has 10 segments and 11 pairs of limbs, long papillae on body and limbs, and 10 pairs of plates (sclerites) on the dorsal of the body. Anterior to the first pair of light sclerites

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Fig. 56 SEM images of isolated sclerites of Microdictyon sp. photographs (a, b) of laterally (c) and dorso-laterally compacted (d) complete specimens of Microdictyon sinicum from Early

Cambrian Moatianshan Shale. Scale bars = 100 μm (a, b) and 1 cm (c, d) (a, b, courtesy of X. G. Zhang)

is a short, smooth, barrel-shaped head, with a mouth opening at the terminus. A pair of head appendages (antennae) extends anteriorly from the lateral rear portion of head. The cylindrical trunk bears ten pairs of unjointed limbs and the same number of dorsolateral sclerites dorsal to the limbs. Each sclerite has an oval base attached to the trunk and a conspicuous spine-like structure protruding dorsally near the dorsal margin of the sclerite. The trunk is annulated, with four annulations per segment, but three in the last segment. Each annulation has approximately ten or more conspicuous cirri aligned transversely in the middle of each annulation. The limbs are relatively stout and annulated, with a pair of terminal claws, directed posteriorly except for the last pair, which is oriented anteriorly. Each limb has 10–12 annulations. Each limb annulation had two cirri, protruding from both the outer and inner sides of the limb. A slender simple gut extends through the entire length of the body to both termini. L. longicruris is small (c. 2 cm) (Figs. 60 and 61). Its barrel-shaped head has a pair of appendages extending anteriorly. The trunk is cylindrical, supported by

13 pairs of appendages. The segments are wider in the central part, but narrow both anteriorly and posteriorly. There are eight trunk annulations per segment; this decreases to three both anteriorly and posteriorly. The trunk annulations are subequal in width, but are much wider near to the boundary of the two adjacent segemts in order to bear three small dorsal sclerites. The trunk limbs are slender, tapering distally, with 4–5 terminal claws. They are faintly annulated, with a pair of setae on each annulation. The setae are directed both anteriorly and posteriorly. The two species C. catenulum (Figs. 62 and 63a–c) and H. fortis (Figs. 64 and 65) represent the twosegmented-head taxon. They display an advanced body plan among the stem-lineage panarthropods. C. catenulum is small, at 3 cm in length. The body is cylindrical and bipartite. The head is small, with an elongate oval shape, and a mouth opening anterioventrally. It has two pairs of head appendages, extending anteriorly from the narrow rear portion of the head. The cylindrical trunk is supported by 23–25 pairs of unjointed limbs and is armed with the same number of

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Fig. 59 Onychodictyon ferox from Early Cambrian Maotianshan Shale. (a, b) part and counterpart of a laterally compacted trunk. Scale bar = 1 cm

Fig. 57 Restoration (a) and photographs of laterally compacted (b) and latero-dorsally compacted (c) Paucipodia inermis from Early Cambrian Maotianshan Shale. Scale bar = 0.5 cm

Fig. 58 Restoration of Early Cambrian Onychodictyon ferox

sclerite pairs, dorsal to the limbs. The limbs are short with two distal claws directed posteriorly, except for the last pair, which is directed in the opposite direction. The sclerites are in a peltate form in the adult (Fig. 63a) but are V-shaped in the juvenile (Fig. 63c), with the narrow angle directed ventrally. The gut is a simple, straight tube that opens at both ends. H. fortis in the Maotianshan Shale resembles the type species Hallucigenia sparsa (Walcott 1911a; Conway Morris 1977c) from the Middle Cambrian Burgess Shale, in many of its characters including the shape of its sclerites and the numbers of its head and trunk appendages.

Fig. 60 Restoration of Early Cambrian Luolishania longicruris

However, the oval-shaped head of H. fortis differs significantly from that of H. sparsa as it resembles the elongated head of M. sinicum, narrowing anteriorly. This tail-like “head” has been broadly accepted as a tail. In addition to this anterioposterior reversal, the dorsal spine-like sclerites in H. sparsa were thought to be ventral limbs, so the animal was previously interpreted as being in an upside-down position. The animal was popularized with a reconstruction resulting from

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Fig. 62 Restoration of Cardiodictyon catenulum

Fig. 61 Luolishania longicruris from Early Cambrian Maotianshan Shale showing anteriorly extended head appendages (a), annulated appendages with a pair of setae in each annulation (b), a simple straight gut (a, b) and each trunk segment bearing three small dorsal sclerites (a) (b, courtersy of XG Hou). Scale bar = 0.5 cm

misinterpretation (Fig. 66). The complete specimens in the Maotianshan Shale clearly document the body form of H. fortis as small (2–3 cm long) with a characteristic two-segmented oval-shaped head, a trunk supported by seven pairs of slender limbs, and was armed with the same number of spine-like sclerites (Figs. 64 and 65). The inner side of the head is kidney shaped, with a narrow neck-like rear portion. Two head appendages extend anteriorly from the rear portion of the head; they are fairly slender and relatively long, extending far beyond the front margin of the head (Fig. 65a). Like Cardiodictyon, the mouth of H. fortis also opens anterioventrally. The trunk is slender, thick in the middle, and narrowing both anteriorly and posteriorly. Horn-shaped sclerites ornamented with fine striatae, extend dorsolaterally from the trunk, with the concave side directed anteriorly in the anterior sclerites and posteriorly in the posterior ones. The tardipolypods were interpreted to have been epibenthic animals living on the surface of semi-firm substrates. It is interpreted that most species used their limbs to raise their bodies above the sea floor. L. longicruris was the exception by spreading its limbs nearly

horizontally, keeping its body close to the sea floor. The muscular body wall of the animals is like that of living soft-bodied bilateral worm-like organisms, arranged in circular and longitudinal muscle layers. The alternating contraction of the longitudinal and circular muscles around an enclosed fluid-containing space produces locomotion. The rearward-directed terminal claws favour forward locomotion; the claws in the posterior limbs anchor the organism to the surface, while the body is elongated with the contraction of the circular muscles. Alternatively, the claws in the anterior limbs anchor the animal while the body is shortened by the contraction of the longitudinal muscles. The anterior forward-pointing claws on the last pair of limbs suggest that the animal was capable of backward locomotion by anchoring the claws in the last pair of limbs while the longitudinal muscles contracted. Microdictyon and Paucipodia are both found on the dorsal surface of the pelagic medusiform soft-bodied organism known as Stellostomites, suggesting that it was a pseudopelagic organism (Fig. 67). Anterior of long, slender appendages are usually directed anterilry, favouring their adhesive attachment to the pelagic host. The small terminal mouth suggests that tardipolypods fed on microscopic bacteria, algae, and fine organic detritus. Some tardipolypods, such as Microdictyon and Paucipodia, may have fed on the body fluids of their host, Stellostomites, by penetrating the body wall of the host with an oral stylet-like structure, although we have not yet found evidence of stylets. The narrow anterior end of the elongated

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Fig. 63 Cardiodictyon catenulum from the Early Cambrian Maotianshan Shale. (a) lateral compaction of a complete specimen showing an oval head with two head appendages, a simple straight gut and shield-shaped sclerites; (b) laterally compacted

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head and anterior portion of trunk showing two pairs of head appendages; (c) laterally compacted juvenile specimen showing triangular sclerites. Scale bars = 1 cm (a), 0.5 cm (b, c)

Fig. 64 Restoration of Early Cambrian Hallucigenia fortis

head of M. sinicum may have allowed the animal to penetrate the soft mud, to feed on buried carcasses. Sclerites are present in most tardipolypods, except Paucipodia. Although the sclerites vary in both morphology and placement, they are, interestingly, all restricted to the trunk, occurring in a metameric pattern. Scleritization is deeply rooted in the stem-lineage panarthropods and is not a novel attribute of arthropod evolution. Sclerites possibly played a protective

Fig. 65 Hallucigenia fortis from Early Cambrian Maotianshan Shale, showing oval head with two pairs of head appendages (a, b), seven pairs of trunk spine-like sclerites and appendages (b). Scale bar = 1 cm

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Fig. 66 Fanciful, upside-down reconstructions of the Middle Cambrian Hallucigenia sparsa (reproduced from the poster in front of the administrative centre at Park Field, Canada)

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Fig. 67 Medusiform Stellostomites eurorphus and associated Microdictyon sinicum. (a) restoration of pseudopelagic Microdictyon sinicum (b). Scale bar = 1 cm (a)

role and acted as sites of muscle attachment. The sclerites in both Hallucigenia and Onychodictyon have a conspicuous spine-like extension; their protective role seems clear. The proximal base of the horn-like structure is highly ridged, apparently a site of muscle attachment, although the surface of the proximal base is small. The sclerites in Microdictyon are exceptionally complex, made up of over 100 repeating cylindrical units that extend vertically through the sclerites and resemble the ommatidia of the compound eyes of arthropods (Fig. 56a, b; Fig. 68). The repeating units are hollow; these structures may represent dissolved calcite crystal cones, separated by solid cuticular walls (Zhang and Aldridge 2007). The interspaces between the crystal cones are spiky, mushroom-shaped structures, and the crystal cones have a convex outer surface (Fig. 68). Although the sclerites in Microdictyon may have acted as sites of muscle attachment and possibly in protection (Zhang and Aldridge 2007), their striking

Fig. 68 Enlargement of sclerites in Microdictyon sinicum showing convex outer surface of the cylindrical units and nodular-like structure in the interspaces between the cylindrical units. Scale bar = 0.2 cm

similarity to the compound eyes of trilobites suggests that they were possibly visual organs. Liu and her collaborators (Liu et al. 2004) recently erected a new lobopodian species, Miraluolishania haikouensis, representing an intermediate form between lobopodians and arthropods. M. haikouensis has small, paired, hardened sclerites, placed dorsally on each pair of appendages, and the “possible dorsal sessile eyes” seem to represent the anteriormost paired sclerites. M. haikouensis shares features with Luolishania, including its body form, number of appendages, and small, dorsally situated, hardened sclerites. In 2009, Chen reinterpreted M. haikouensis as a possible synonym or sister species of L. longicruris.

The Evolutionary Transition from Walking Worms to the First Arthropods The lack of fossil evidence of the first arthropods has resulted in much controversy surrounding studies of arthropod origins. Most researchers agree that the ancestor of the arthropods is found among the least complex walking worms. Among the fossil assemblage of arthropods in the Maotianshan Shale deposits is a group of arthropods recently defined as the stem group of the arthropods, called proarthropods (Chen 2004), including Fuxianghuia protensa (Hou 1987), Shankouia zhenghei (Waloszek et al. 2005, 2007), and Chengjiangocaris longiformis (Hou and Bergström 1991). F. protensa is the first of these proarthropods described from a basal position among the Euarthropoda (Chen et al. 1995b) (Fig. 69). It has a head composed of only two tergite-bearing segments (Chen et al. 1995b; Hou and Bergström 1997), and the second tergite is interpreted as bearing two pairs of

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Fig. 69 Fuxianhuia protensa from the Early Cambrian Maotianshan Shale showing a small visual segment (a, c, d) with stalked eyes (a–d); an antennal segment bearing a relatively large head shield (b–d), a pair of short stout antennae

(a, c, d) and a pair of crescent-shaped diverticula lying below the head shield but above the tergite (c, d). Scale bars = 0.2 cm (a, c), 1 cm (b, d)

appendages, representing two segments. However, the identity of the “second pair of limbs” is refuted by evidence of their internal location between the dorsal and ventral cuticles (Waloszek et al. 2005; Fig. 69d). The authors have reinterpreted them as a pair of diverticula in the anterior region of the digestive tract. The head is reinterpreted as two segmented, with an anterior visual segment and a posterior antennal segment. A similar two-segmented head is also recorded in both C. longiformis and S. zhenghei. The discovery of a two-segmented head, together with lobopod-like trunk limbs, among the Proarthropods is of great interest, presenting a

novel perspective on the evolutionary origin of the arthropods (Fig. 70). The anatomical characters of the proarthropod group establish a bridge linking the tardipolypods and the euarthropods. The twosegmented head of the first arthropods suggests that the arthropod ancestor is among the limb-bearing worm-like organisms resembling the Hallucigenia + Cardiodictyon clade, and not among the living walking worms. The extant walking worms comprise two phyla (Onychophora and Tardigrada). The phylum Onychophora (or velvet worms) is characterized by a cylindrical body, supported by 13–43 pairs of trunk appendages. The head consists of three head

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Fig. 70 Schematic restoration of the possible arthropod bauplan. Abbreviations: ant, antennae; br, brain; en, endopod; ex, exopod; gu, gut; gud, gut diverticulum; h, heart; ins, inserter;

mo, mouth; nc, neural cord; se, stalked eyes; tas, tergite of antennal segments; tos, tergite of ocular segment; ts, tergite of trunk segments (adapted from Waloszek et al. 2005: Fig. 4)

segments, each carrying a pair of modified appendages corresponding to sensory antennae on the first pair, claw-like mandibles on the second pair, and oral papillae on the third pair. Tardigrades, generally known as “water bears”, are microscopic walking worms with a segmented trunk and a short head. The head may have three segments with a terminal mouth and the trunk has 4–5 segments. The trunk legs are short and stubby, with 4–8 retractile claws or an adhesive disc at the tip of each leg. These two groups are highly modified walking worms with three-segmented heads and are unlikely to represent arthropod ancestors. F. protensa is large, with an approximate length of 10 cm (Figs. 69 and 70). The head consists of a small visual segment, with an oval tergite, jointed posteriorly to the antennal segment (Fig. 70) over which a pair of stalked eyes extends ventrolaterally. The antennal segment is relatively large and covered dorsally with a fairly large tergite extending posteriorly far beyond the head–trunk boundary above the three anterior trunk segments. Extending ventrolaterally from the antennal segment is a pair of short, stout antennae. A pair of crescent-shaped structures extend lateroposteriorly from the second segment on the internal surface of the tergite. Ventral to the structure is a membrane interpreted as a sternite, a structure previously thought to be monoramous limbs, but recently reinterpreted as diverticulae extending from the mid

gut in the second segment. The trunk is differentiated into three parts: the thorax, the abdomen, and the telson. The thorax consists of 16–17 segments, each carrying a pair of biramous limbs divided longitudinally into a pair of pleural lobes, and an elongated median axial region that narrows slightly rearward. The pleural lobes are wider in the middle portion but narrow both anteriorly and posteriorly. The cylindrical endopod of the biramous appendage is unjointed and closely annulated, with more than 20 annulations (Hou and Bergström 1997; Bergström and Hou 1998). The exopod is large and flap-like, adorned with short setae. The abdomen is cylindrical, made up of 14 segments lacking appendages. A small caudal tail consists of a pair of flattened paddle-like structures (uropods, similar to those in crustaceans) and a spine-like telson. Newly discovered S. zhenghei is known only from Shankou, Anning (Chen 2004; Waloszek et al. 2005). The species is named after the great navigator and explorer of the Ming Dynasty, Zhenhei, who was born near the fossil site in Shankou village. The animal (Fig. 71) on average is 5–6 cm long, reaching a maximum of 7.5 cm. The head resembles that of F. protensa; it has two segments, a small first segment articulated posteriorly with the second segment. The second segment has a large tergite, extending posterior to the six anterior trunk segments. The antennae on the second segment are short and stout, comprising 14–16

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Fig. 71 Shakouia zhenghei from the Early Cambrian Maotianshan Shale. (a) dorsal view of a complete specimen; (b) enlargement showing multiple annulated tubular-shaped

limbs; (c) enlargement showing flap-like exopods and tubular endopods. Scale bars = 1 cm (a), 0.5 cm (b), and 0.2 cm (c)

segments with no setae. Unlike F. protensa, the trunk of this species is not differentiated into a limbless abdomen in its rear portion, but comprises 43 segments, each bearing a pair of biramous appendages. Like F. protensa, it is divided longitudinally into pairs of pleural lobes and a median axial region. The pleural lobes narrow anteriorly and posteriorly in its anterior and posterior portions, respectively, but the pleural lobes in its main middle portion are relatively wider. The trunk appendages resemble those of F. protensa, comprising large, flap-shaped exopods with short setae at their margins. The endopods are tubular, with at least 17 annulations (Bergström and Hou 1998). The caudal tail is large, comprising a pair of large, flattened paddle-like structures and a spine-like telson. A pair of small, flattened paddle-like structures is also present behind the larger uropods.

Affinities and the Ground State of the Arthropods Paired, jointed, segmented appendages have previously been accepted as one of the key characters defining the arthropods. The term “Arthropoda” originates from the Greek αρθρov (arthron) meaning “joint”, and πoδóς (podos) meaning “foot”, together meaning “jointed feet”. However, the proarthropods have unjointed limbs, inconsistent with the definition of the Arthropoda, although they share the characteristics of a segmented body and a chitinous exoskeleton. The proarthropods have a bi-segmented head, corresponding to the pre-oral part of the arthropod head, the post-oral portion, consisting of at least three segments. Interestingly, the head segmentation shows a close

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affinity to that of a walking, worm-like stem group of Panarthropods, the Hallucigenia–Cadiodyctyon clade, sharing the same number of head segments. The proarthropods most probably represent the missing historical link between the walking worms and the arthropods, thus shedding new light on the evolutionary origins of the arthropods. Despite sharing similar head segmentation, there is a large morphological gap in the heads of the wormlike ancestors and the first arthropods (exemplified by the proarthropods). The transition from the twosegmented head of the worm-like ancestors to the first arthropod head required quantum leaps through multiple, synchronous events, including the evolution of the first head appendages into stalked eyes; the specialization of the second head appendages into sensorial organs, known as “antennae”; and the displacement of the mouth to a ventral position in the antennal segment. The head in the basal arthropods, as exemplified by the proarthropods, is small and two segmented, with an anterior visual segment and a posterior antennal segment. It has been proposed that the anterior of ancestral arthropods, known as the “acron”, was non-segmented. The acron hypothesis is refuted by the study of proarthropods. Head sensory organs consist of a pair of stalked compound eyes in the first segment and a pair of short and segmented antennae. Apparently, image-forming eyes had not yet appeared in the tardipolypods; they relied on a simple visual system, known as “eyespots”. Some authors have reported eye-like structures in Luolishania (Liu et al. 2004, 2008) but these may, in fact, be dorsal sclerites. The appearance of compound eyes in all three proarthropod species suggests that compound eyes are apomorphic in the arthropods. Whether the original compound eyes were stalked or sessile is an ongoing controversy. The eyes of all proarthropods have a clear, short, tubular stalk. The compound, stalked eye arguably characterizes the ground state of the arthropod eye. Tubular, possibly segmented, eye stalks represent tubular extensions of the body wall, homologous to tubular limbs. This argues for the segmental origin of the anteriormost head region in the arthropods, evolving from the anteriormost, limb-bearing head segment of a worm-like ancestor of the Hallucigenia–Cadiodyctyon clade. The flagelliform antennae have long been accepted as the original arthropod version of the uniramous antennae. Long and multisegmented flagelliform

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antennae occur widely among the trilobites and extant arthropods; it is assumed that the antennae have a sensorial function. The flagelliform hypothesis, however, comes under scrutiny as the proarthropods with short, stout antennae with a limited number (about 15) of segments (Fig. 69a, c). The short, limb-shaped antennae occurring in all proarthropods and in some stem-lineage euarthropods (Canadaspis, Primicaris, the bradoriids, and Ercaia), represent the ground state of the arthropod antennae (cf. Maas et al. 2004). In the ground state of the panarthropods, as exemplified by the tardipolypods, the mouth was situated terminally on the anterior segment. The ventral anterior location of the mouth in Hallucigenia and Cadiodyctyon suggests that the relocation of the mouth has an early history, rooted in the stem-lineage panarthropods. In contrast, the mouth in the ground state of the arthropods, as exemplified by the proarthropods, is located ventrally and opens posteriorly in the rear part of the antennal segment. The displacement of the mouth to a new position represents one of the major events during the evolutionary transition from the worm-like ancestor to the arthropods, although it was initiated in the pre-arthropod evolutionary stage. The looped anterior digestive tract in arthropods argues that the mouth displacement resulted from the curving back of the first head segment. C. catenulum and H. fortis (Figs. 62, 63, 64, and 65 have an expanded and ventrally curving head and an anterior, ventrally situated mouth, representing an early stage of mouth displacement. Scleritization occurs broadly among the stemlineage panarthropods, forming metamerically arranged hard cuticles on the dorsolateral surface (few on the dorsal side) of the trunk, but the main part of the body remains soft. Arthropodization is characterized by the formation of hard, jointed, segmented cuticles that cover the entire dorsal surface, whereas the trunk limbs remain soft. This event, exemplified in the proarthropods, was the evolutionary development allowing for the origination of the arthropods. The formation of jointed sclerites had far-reaching effects on the evolutionary changes in the anatomy, physiology, ecology, and behaviour of the arthropods (Ruppert et al. 2004). The ground state of the panarthropod appendages was monoramous and unjointed. The trunk appendages in the arthropod ground state are biramous but their endopods remain unjointed (Fig. 71). The head

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appendages are modified into sensory organs, the stalked eyes and antennae, although they remain in the monoramous state. The exopods are an evolutionary novelty in the arthropods and the first exopods, exemplified in the proarthropods, were flap-like and without gill-like structures, apparently not used for gas exchange but rather in swimming locomotion. The exopods are extended pouches of the body wall adjacent to the base of the limbs. Morphologically, they resembled insect wings, suggesting that the developmental process of the exopods is similar to that of wing development. One might suggest that co-ordinating a genetic cassette for development of the insect wing is very ancient, used by the first arthropods in exopod development and later recruited by insects for wing morphogenesis. The ground plan of the arthropod trunk appendages is biramous, as exemplified by S. zhenghei and possibly C. longiformis. There is little differentiation among the different segments, except in F. protensa, in which the trunk is differentiated into a limb-bearing thorax and a limbless abdomen. The limbless abdomen is a secondarily derived feature, probably the result of the repressed expression of the Distalless gene. The ground plan of the arthropod endopod is a simple tubular form, consisting of multiple segments. It is not very different from the ground plan of the panarthropod limb, except for the pivotal joints between two adjacent segments in the endopods of the arthropod ground plan. The presence of pivotal joints suggests the presence of intrinsic muscles in the first arthropod endopod.

Evolutionary Transition from the First Arthropods to the Euarthropods Waloszek established the Euarthropoda to include all extant arthropods and a number of extinct arthropod lineages, all characterized by a composite head and bipartite trunk limbs (composed of an expanded basipod and with six or fewer segments in the distal portion) (Waloszek 1999; Maas and Waloszek 2001). A monophyletic status was proposed for the Euarthropoda by the authors. The significant morphological gap between the proarthropods and euarthropods suggests the presence of an intermediate evolutionary stage. The Lower Cambrian Maotianshan Shale has yielded diverse

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extinct arthropods that fill the morphological gap between the first arthropods and the euarthropods. These intermediate forms represent different evolutionary stages towards the Euarthropoda in both the head and appendages. For instance, some forms have possibly proarthropod-like two-segmented heads but their trunk appendages are tubular and multisegmented. Some forms have a composite head and tubular, multisegmented limbs. Interestingly, the limbs in some forms have a bipartite design but their basipod is multisegmented. The evolutionary transition towards the euarthropods was much more complex than previously thought and was marked by two parallel events, cephalization and arthropodization. These two events occurred in asynchronous and step-wise ways. During this transformation, the antennae on the antennal segment either remained unchanged or were specified as a flagelliform sensorial organ or a raptorial limb-like feeding organ. The development of the raptorial limb-like antennae was the key evolutionary novelty that led to the origin of the Chelicerata. The ground state of the post-oral head of the Euarthropoda, exemplified by the stem-lineage euarthropods in the Maotianshan Shale, is a threesegmented form, and each of the segments carries a pair of indefinitely differentiated biramous appendages, appearing to be homologous to the postoral head appendages, and trunk appendages. The modification of the post-oral head appendages into feeding organs is the key evolutionary event leading to the Crustacea. This modification occurred in multiple asynchronous steps. As exemplified by Ercaia minuscule from the Maotianshan Shale, the modification of the first pair of post-oral biramous appendages into the second antennae was the first event on the path to the Crustacea (Chen et al. 2001), suggesting that the Crustacea is deeply rooted in the evolutionary transition towards the first Euarthropoda. The design of the post-antennal limbs of the euarthropod ground plan has been defined as bipartite, with an expanded proximal portion (called the “basipod”) and a distal portion (consisting of seven or fewer segments). The bipartite post-antennal limb is associated with feeding and locomotion functions (Waloszek and Müller 1990; Waloszek 1993). It has been interpreted as monophyletic and the key novel event in the origin of the Euarthropoda. The Lower Cambrian Maotianshan Shale has yielded many extinct, morphologically disparate arthropod groups,

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with tubular multisegmented post-oral limbs. They include the first Mandibulata (E. minuscule), the stem lineages of the Chelicerata (Leachoilia, Fortiforceps, and Tanglangia), and other extinct euarthropods (Saperion, Canadaspis, Isoxys, bradoriids, and Primicaris). Among the intermediate forms, Canadaspis is a macroscopic bivalved arthropod that is well represented in the Middle Cambrian Burgess Shale (Briggs 1992, 1994; Briggs et al. 1994), but is much less common in the Lower Cambrian Maotianshan Shale where it is represented by Canadaspis laevigata (Hou and

Bergström 1991; Chen 2004) (Fig. 72). The body of the species consists of a small head, thorax, and abdomen, mostly covered by a large, unjointed, bivalved carapace, except for its abdomen, which is not covered by carapace. Its head probably resembles that of the proarthropods, with two segments and a pair of stalked eyes on the first segment and a pair of short antennae on the second segment. The carapace may be comparable to the large head shield of the proathropods, both representing a modified giant second tergite. The thorax comprises about 10 segments, each carrying a pair of biramous appendages. The abdomen is

Fig. 72 Canadaspis laevigata from the Early Cambrian Maotianshan Shale showing its oval bivalved carapace (a, c–e) and elongate body (b, e) attached to the anterior part of the carapace—with short front portion (a, c–e); the thorax, a

region free from the carapace (but beneath it), bears biramous appendages (a–e); the abdomen was legless, not covered by the carapace (a, c–e). Scale bar = 1 cm (a, c–e), 2 cm (b)

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rounded and legless, consisting of about ten closely arranged segments, each with a pair of short caudal spines. The exopods are flap like, with short setae at the margins. The endopods are not well preserved in the Lower Cambrian Maotianshan Shale. They probably resemble those in the Middle Cambrian Burgess Shale species Canadaspis perfecta, which has 14 limb segments and is bipartite, with an expanded proximal portion (formed by seven proximal limb segments) and a slender distal portion. Primicaris lavaformis was named by Zhang et al. (2003), and represents larva-like microscopic arthropods of 0.7–5 mm in length (Figs. 73 and 74). The body is entirely covered with a dorsal shield and is differentiated into two parts, the anterior and posterior parts, corresponding to the head and trunk, respectively. The head is broadly rounded with a smooth margin and forms a conspicuous, relatively broad, cephalic doublure fold. It represents the anterior 1/3 to 2/5 of the body, with an elongated hypostome that joins the doublure on its anterior margin and extends across the entire length of the head. A pair of elongated antennae extends anteriorly from the lateral surfaces of the hypostome at 3/5 of its length from the front. The antennae consist of about 15 segments, each carrying conspicuous setae at their joints. The head possibly has two segments. The trunk is characterized by a serrated margin on the dorsal shield, with approximately 15 segments, and each serration of the dorsal shield corresponds to a trunk segment. The trunk appendages

Fig. 73 Restoration of Early Cambrian Primicaris lavaformis

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are biramous, with elongated and gill-bearing exopods. The endopods are sub-tubular in form and multisegmented. Cindarella is a mono-specific genus represented by Cindarella eucalla (Chen et al. 1996; Ramsköld et al. 1997; Chen 2004), known from a few wellpreserved specimens (Figs. 75 and 76). The head shield is hemispherical in outline and extends posterior to the anterior part of the trunk. The head segmentation is not yet clear, but it is considered to have three postoral segments. The antennae are whip like and extend anteriorly from the sides of the anterior part of the hypostome. The eyes are large and stalked. The trunk is composed of 26 segments and the anterior five segments are “shadowed” by the head shield. The trunk appendages (including the post-oral head appendages) are all biramous. The exopods are gill-bearing and elongated. The endopods are tubular, consisting of 13 segments and a distal claw. Saperion is a large, rarely occurring arthropod (12 cm long) (Hou et al. 1991; Chen et al. 1996; Hou and Bergström 1997; Chen 2004). The body is totally covered by a single dorsal shield, which is elongated with a broadly rounded margin both anteriorly and posteriorly (Figs. 77 and 78). The large dorsal shield is folded into a wide W-shape transversely and thus strengthened. The first segment of the body has a pair of stalked eyes ventrally and the second segment has a sub-square hypostome and a pair of short, bent antennae, extending laterally and posteriorly from the lateral

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Fig. 74 Photographs of Primicaris lavaformis from the Early Cambrian Maotianshan Shale showing its dorsal shield differentiated into anterior and posterior parts (a–f, d–h); the anterior part was broadly rounded with smooth margin and had a conspicuous relatively broad cephalic doublure (a–c, FVH) with an elongate hypostome joined to the anterior margin of doublure and extending across the entire length of the anterior part (a–b), a pair of elongate antennae (a, f–g) extending anteriorly from

the lateral sides of the hypostome at about 3/5 of its length from the front (f); the posterior part is serrated (a, e, f) and possesses approximately 15 segments; each serration of the dorsal shield corresponds to a trunk segment (a, d, e); the biramous trunk appendages have elongate, gill-bearing exopods and multisegmented sub-tubular endopods (a, c–h). Scale bars = 1 mm (a–e), 0.5 mm (h)

margins of the hypostome. The post-oral part of the body carries 26 pairs of biramous appendages. The exopods are gill-bearing. Interestingly, its endopods are bipartite, composed of an expanded proximal portion and a slender distal portion. The proximal portion has three segments and their inner margins are serrated. The distal portion consists of six segments with a terminal claw. Bradoriids are small, bivalved arthropods (2–4 mm long) of uncertain affinity and were an important

component of the Cambrian faunal assemblages before their disappearance in the middle Ordovician (Fig. 79). Bradoriids are currently thought to be a possible sister group of the Crustacea and the phosphatocopids (a sister group to the crown group, Eucrustacea). Their body is entirely covered by a bivalved carapace, which is preserved as either disarticulated or articulated “butterfly”-like valves. Soft-part preservation is uncommon. The bradoriids in the Maotianshan Shale are not only common but also diverse. Kunmingella

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Fig. 77 Restoration of Early Cambrian Saperion glumaceum

Fig. 75 Restoration of Early Cambrian Cindarella eucalla. (a) dorsal view; (b) ventral view

douvillei is the dominant form; its “butterfly”-like articulated carapace is usually seen on the bedding plane in an aggregated state (Fig. 80). The few specimens preserved with soft parts show that the endopods are tubular and multisegmented (Fig. 79c). Some specimens retain clutches of eggs in their appendages (Fig. 79a, b), suggesting that the eggs of the animals were deposited and brooded within egg sacs attached to the appendages. Bradoriids represent a major element of the primary consumers in the Maotianshan biota and the undigested residues in some giant fossil coprolites predominantly contain small carapaces related to bradoriids

Fig. 76 Cindarella eucalla from the Early Cambrian Maotianshan Shale. (a, b) part and counterpart of holotype; (c) dorsal view of a nearly complete specimen. Scale bars = 1 cm (a, b), 2 cm (c)

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Fig. 78 Saperion glumaceum from the Early Cambrian Maotianshan Shale. Scale bar = 2 cm

(Fig. 80b), suggesting that bradoriids were the main diet of many animals, including some unknown giant predators.

Extinct Stem-Lineage Euarthropods The euarthropods in the Maotianshan Shale are diverse, including several extinct major groups such the trilobites, trilobitomorphs, and naraoiids. They share several key characters, including a fivesegmented head; post-oral appendages that are all biramous and homologous other than in their morphology; and endopods in the post-oral appendages that are bipartite, with an expanded basipod and a sixsegmented distal portion. However, these three groups are significantly different from one another. The trilobites are characterized by a mineralized exoskeleton and sessile dorsal eyes, three clear axial lobes, and a

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tripartite body (a head, a jointed thorax, and a fused pygidium). The trilobitomorphs resemble trilobites in sharing a tripartite body, but they differ from trilobites in their non-mineralized exoskeleton and their stalked and ventrally situated eyes. Naraoiids, including Misszhouia and Naraoia, are characterized by their lack of eyes and a bipartite body composed of a head and trunk. The trilobites are widely accepted as the dominant components of the macroscopic fauna. Surprisingly, they are minor components of the Maotianshan Shale, accounting for only approximately 5% or less of the number of species and individuals, although their preservation is potentially high. This suggests that the variance in the potential preservation of the organisms plays a critical role in their biased preservation. These trilobites include the following species: Eoredlichia intermedia, Yunnanocephalus yunnanensis, Wutinggaspis tingi, and Kuanyangia pustulosa. Their ventral soft parts are presumably often preserved but these soft parts under the hard dorsal exoskeleton are extremely difficult to expose during mechanical preparation. E. intermedia is a well-known trilobite (Figs. 81, 82, and 83), with a total body length of more than 20 cm. Its cephalon has a conical glabella, incised with three clear furrows. The furrows probably correspond to the post-oral head segments, suggesting three post-oral head segments. The antennae are whip like, extending laterally from the glabella for one-fourth of its length (Fig. 83). The insertion sites of the antennae, corresponding to the antennal segment, are situated slightly anterior to the anterior glabella furrow. The antennae extend anteriorly along the ventral surface and anteriolaterally beyond the front margin of the cephalon. The sessile eyes are large and crescent shaped, with an anterior margin located near the front margin of the glabella and ending posteriorly, at a position equal to the posterior glabella furrow. The free cheek has a long genal spine extending posteriorly to a level equivalent to the posterior margin of the trunk. The thorax has 15 segments and its ninth segment in the axial lobe has a long spine, extending posteriorly, with a length approximately equal to the length of the body. The pygidium is small. Y. yunnanensis (Fig. 84) is small, only a few centimetres long, characterized by a small free cheek that is narrow and spineless, and a subquadrate glabella with a wide preglabella field, which has three

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Fig. 79 Kunmingella douvillei from the Early Cambrian Maotianshan Shale. (a, b) dorsal (a) and side view (b) of specimens showing numerous eggs attached to appendages; (c–e) side

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(c) and dorsal view (d, e) showing multisegmented appendages. Scale bar = 2 mm

Fig. 80 Aggregated “butterfly” like valves of Kunmingella douvillei on a bedding plane (a) and a large coprolite containing mainly small carapaces related to bradoriids. Scale bars = 0.5 cm (a), 0.2 cm (b)

conspicuous furrows. The sessile eyes extend forward posteriolaterally from the lateral surfaces of the anterior glabella. The thorax consists of 14 segments and the pygidium is small.

K. pustulosa (Figs. 85 and 86) is a large trilobite, 10 cm long, characterized by a short cephalon (one-fifth of the body length), which bears a pair of wide free cheeks with short genal spines. The

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Fig. 81 Restoration of Early Cambrian Eoredlichia intermedia

hypostome is expanded anteriorly, with a rostral plate directly meeting the doublure. The gut has pairs of segmentally arranged diverticulae. Based on the evidence of the diverticulae, there are three post-oral head segments, coincident with the number of glabella furrows. The thorax consists of 16 segments and the pygidium is small. The dorsal surface bears densely arranged, small but distinct nubbles. The trilobitomorphs in the Maotianshan Shale include Kuamaia lata (Hou 1987; Chen et al. 1996; Hou and Bergström 1997; Chen 2004), Retifacies abnormalis (Hou et al. 1989; Hou and Bergström 1997; Chen 2004), and Acanthomeridian serratum (Hou et al. 1989), which share several important characters including a tripartite body corresponding to a relatively short five-segmented head with a pair of ventral stalked eyes, the thorax, and the pygidium, and a non-mineralized exoskeleton. Kuamaia is a giant, with a maximal length of 40 cm. The head is small, with five segments: a small visual segment carrying a pair of stalked lateral eyes, a relatively larger antennal segment with a ventral hypostome and a pair of whip-like

Fig. 82 Eoredlichia intermedia from the Early Cambrian Maotianshan Shale displaying a complete caudal spine. Scale bar = 2 cm

antennae extending from the lateral surfaces of the anterior part of the hypostome, and three post-oral segments, each bearing small biramous appendages. The thorax has seven segments and the pygidium has five pairs of appendages. The visual segment is not fused but jointed to the head shield. R. abnormalis (Figs. 87 and 88) is relatively large, with a maximum length of 30 cm, and is characterized by a fairly small cephalon (only one-eighth of the body length) with five segments, like that of Kuamaia. The thorax has ten segments. The pygidium is relatively large, with up to five indistinct segments, and with multiple spines on the peripheral posterior margin. The almost smooth surface is decorated with a faint polygonal ridged structure. The post-oral appendages are

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

Fig. 83 Eoredlichia intermedia from the Early Cambrian Maotianshan Shale displaying a pair of whip-like antennae. Scale bar = 2 cm

biramous, and with a large plate-like exopod and a stout, seven-segment, bipartite endopod. Among these stem-lineage euarthropods, the naraoiids are well represented by bulk, and their anatomy is well documented. Misszhouia longicaudata (Chen et al. 1997) is an elongated, oval-shaped animal, about 5 cm long (Figs. 89 and 90). The bipartite body consists of a distinct head and a carapace-covered trunk. The head is covered dorsally by a hemispheric head shield, with an oval hypostome complex on the ventral side. A pair of whip-like antennae extend from the anteriolateral surfaces of the hypostome. The animal has no eyes, but has three frontal organs anterior of the hypostome. The three post-oral head segments are defined by the presence of three post-oral biramous appendages. The thorax has 21 pairs of biramous appendages. Each exopod consists of a slender jointed shaft, bearing filaments, with a small distal lobe. The endopods are distinctly

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bipartite, with an expanded proximal portion (the basipod), with serrations on its inner surface. The distal portion consists of six segments with a terminal claw. The bipartite Naraoia (Figs. 91, 92, and 93) is a close relative of Misszhouia. It is common in the Maotianshan Shale, represented by M. or N. spinosa (Zhang and Hou 1985). It ranges from 1 to 4 cm in length. The head shield is hemispheric; facial sutures appear to be marginal. The head shield extends posteriorly beyond the posterior margin of the head. A pair of antennae extends laterally, rather than anteriorly as they do in Misszhouia. A pair of long, ramifying, distensible diverticulae occurs along the midgut, possibly functioning in both food storage and digestion, as suggested by recent analogues. The trunk is covered dorsally by a carapace and consists of approximately 14 segments. The pygidium may bear a pair of distinct rear lateral spines and three small lateral spines. Naraoia is thought to have lived in water-saturated soft mud and was an opportunistic intermittent feeder. The animals are usually preserved in an enrolled state, with the head parallel to the bedding plane and the thorax extending vertically deep into the surface. The enrolling behaviour may indicate that they could dig into the soft substrate to exploit a potential food source or to protect the organs on the underside of the cephalon from the fine mud and from predation.

Fossils Related to the Evolutionary Transition Towards the Mandibulata The extant arthropods, including the Crustacea, Hexapoda, Myriapoda, and Chelicerata, can be grouped into two deeply rooted clades, the Mandibulata and the Chelicerata. The extant clade Mandibulata is composed of the Hexapoda, Myriapoda, and Crustacea. The head segmentation and related appendages of the Hexapoda and Myriaopoda are homologous to those of the Crustacea, except for the first post-oral segment, which is known as an “intercalary” segment rather than the second antennal segment. Until recently, the intercalary segment has long been regarded as a structure without an appendage, but the labrum has been reinterpreted as a fused pair of appendages of the intercalary segment (Finkelstein and Perrimon 1991; Popadic et al. 1998; Boyan et al. 2002) and the head has been reinterpreted

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Fig. 84 Restoration (a) and photograph (b) of Yunnanocephalus yunnanensis from the Early Cambrian Maotianshan Shale. Scale bar = 5 cm

Fig. 85 Restoration of Early Cambrian Kuanyangia pustulosa

Fig. 86 Kuanyangia pustulosa from the Early Cambrian Maotianshan Shale. Scale bar = 2 cm

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

Fig. 87 Restoration of Early Cambrian Retifacies abnormalis. (a) dorsal view; (b) ventral view

as having six segments (Zacharias et al. 1993; Minelli 2001). The six segments of the insect head are (from anterior to posterior) the ocular, antennal, intercalary, mandibular, maxillary, and labial segments. The insect head segmentation and the related structures show striking homologies to those of Crustacea, suggesting that the insects (possibly including the Myriapoda) originated among the Crustacea or from a crustaceanlike ancestor. The evolution of the second antennae into a feeding organ, known as the “labrum”, with anterior displacement and the fusion of the paired second antennae, was one of the major transitions in the evolution of the insects. E. minuscule (Figs. 94, 95, and 96), known from the Maotianshan Shale, is small (2–4 mm) and represents an ancestral form of Mandibulata (Chen et al. 2001). It has a six-segment head and an elongated, untagmatized trunk bearing serially repeated, biramous appendages (long and segmented endopods and flap-like exopods). The visual segment of the head is small and is covered by a rounded tergite jointed posteriorly to the head shield. A pair of stalked eyes extends ventrolaterally from the visual segment (Fig. 96a, b). The head shield is an elongated oval shape, overlying a pair of antennae and four pairs of post-oral biramous appendages. The

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antennae are elongated, with 10–11 segments and setae in the joints. The first post-oral appendages are highly modified to form large setose fans, which possibly function in feeding and are comparable to the second antennae in living crustaceans (Figs. 95 and 96d). The trunk consists of 13 segments. The appendages, including the trunk and post-oral head appendages, are also biramous and apparently homologous to another, except for the last pair, which is segmented and fringed with setae. The last paired appendages are homologous to the other appendages but are comparable to the uropods seen in various living crustaceans. The endopods of both the trunk and post-oral head are sub-tubiform and consist of 14 segments. The early member of Mandibulata has an isolated visual segment resembling that of the proarthropods and some intermediate forms between the proarthropods and euarthropods. The antennae resemble those in the proarthropods in their general morphology but bear setae, suggesting that they are more advanced than the setae-lacking antennae of the proarthropods. The second antennae are a newly derived character, composed of a relatively small 4- to 5-segment endopod and a large crescent-shaped exopod with prominent setae on its margin. Posterior to the A2, there are usually three biramous head appendages, resembling trunk appendages. The endopods of the post-A2 appendages are tubiform, consisting of 14 segments. The primitive nature of the post-A2 head appendages in E. minuscule suggests that the clade Mandibulata is deeply rooted in the evolutionary transition from the proarthropods to the euarthropods. The recent discovery of an epipodite-bearing eucrustacean Yicaris from Yonshan, Yunnan (not far from the fossil site of E. minuscule), within a horizon almost contemporaneous with the Lower Cambrian Maotianshan Shale (Zhang et al. 2007), indicates that the first appearance of the Eucrustacea was much earlier than we previously thought.

The Stem-Lineage Chelicerata The chelicerates are widely accepted as the unquestioned, basic monophyletic group of the Arthropoda. They share a distinct and conservative body plan, including features such as the prosomal–opisthosomal subdivision and the cheliceral segment, with a pair of morphologically unique chelicerae. The Chelicerata

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Fig. 88 Retifacies abnormalis from the Early Cambrian Maotianshan Shale. (a, b) dorsal view of two nearly complete specimens with preservation of complete segmented caudal spine (b); (c) partially preserved trunk showing trunk appendages; (d) dorsal view of a nearly complete specimen showing polygonal external structure. Scale bar = 1 cm

is named after the pair of modified, uniramous head appendages called the “chelicerae”. The chelicerae consist of only three components: the proximal peduncle and two distal peduncles, forming the chela. The chelicerae have long been regarded as modified second antennae, but on the basis of molecular developmental and neurobiological studies, they have now been reinterpreted as modified first antennae. The ground plan of the chelicerate head consists of a two-segmented anterior head and five-segmented posterior head (Dunlop 1999). On the anterior head, the ocular segment bears dorsal, sessile, compound eyes and the antennal segment bears a pair of anteriorly pointing, raptorial, uniramous appendages, the chelicerae. The posterior head bear five pairs of biramous appendages, as exemplified by the Silurian Offacolus kingi (Sutton et al. 2002).

The large modified antennae known as the “great appendages” have long been recorded from the Early to Middle Cambrian. These “great appendages”, each comprising a proximal arm and a distal claw, are similar to the chelicerae in their general morphology. Despite this similarity, the possible evolutionary relationship between the peculiar Cambrian arthropods with “great appendages” and the Chelicerata was not recognized until the fossil Haikoucaris ercaiensis was found in 2004 (Chen et al. 2004e) (Figs. 97 and 98). The animal, recorded from the Lower Cambrian Maotianshan Shale, has a pair of chelicera-like structures that fill the morphological gap between the Cambrian “great appendages” and the chelicerae of the crown-lineage Chelicerata. The chelicera-like structure consists of a proximal two-segmented arm and a distal

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

Fig. 89 Ventral and dorsal views (a, b) of the Early Cambrian Misszhouia longicaudata

three-fingered claw, resembling the chelicera but has one more segment in both the arm and claw; thus, it is similar to the “great appendage” except that it has one fewer segment than the claws of most Cambrian “great appendage” creatures. Because of their homology to the chelicerae, Chen (2004) referred to these “great

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appendages” as prochelicerae, interpreting them as the precursors of the chelicerae. Further, a group of giant Cambrian predators, known as “anomalocaridids”, also has a pair of large pre-oral “great appendages” (Hou et al. 1999). The “great appendages” of the anomalocaridids are not only much larger than any others but have a multisegmented, spine-bearing arm. However, the small distal claw (usually with four segments) of the anomalocaridids displays a striking resemblance to that in the non-anomalocaridid “great appendage” arthropods. Chen (2004) suggested that the “great appendages” of the anomalocaridids and non-anomalocaridids are closely related and are both representatives of extinct stem-lineage Chelicerata (also referred to as “Prochelicerata”). In addition to their larger “great appendages”, the anomalocaridids have a unique mouth, which is large, ventrally facing, and armed with a ring or several rings of hard, sharp teeth. The Prochelicerata is an extinct animal group, broadly recorded in the Lower to Middle Cambrian from China, Canada, USA, Poland, and Australia. They died out after the Middle Cambrian.

Fig. 90 Misszhouia longicaudata from the Early Cambrian Maotianshan Shale. (a) dorsal view of a nearly complete specimen; (b) bipartite trunk appendage. Scale bar = 1 cm

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Fig. 91 Restoration of Early Cambrian Naraoia spinosa

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of biramous appendages identical to those on the trunk. Their endopod is usually simple and multisegmented, with least differentiation along the main axis (e.g. Fortiforceps foliosa, Leachoilia illecebrosa, and Tanglangia longicaudata), but H. ercaiensis has only seven segments, probably grouped into two functional portions. The primitive design of the limb in most Prochelicerata suggests that the Chelicerata is deeply rooted among the stem-lineage arthropods. The transformation of the short, stout antennae into bipartite prochelicerae was the first key event leading to the evolution of Chelicerata lineage. The transformation of the Prochelicerata head into the Euchelicerata head was marked by two probably synchronous events, the reduction of the procheliceral segments and the recruitment of two more segments from the trunk.

Non-anomalocaridid Procheliceratids

Fig. 92 Naraoia spinosa from the Early Cambrian Maotianshan Shale. Scale bar = 1 cm

The head ground plan in Chelicerata, as exemplified by the Prochelicerata, is a five-segmented model. The five segments are arranged, from anterior to posterior, as the ocular segment, the procheliceral segment, and the three post-antennal segments. Each of the three post-antennal segments has a pair

The diverse non-anomalocaridid procheliceratids are small, only a few centimetres long. In the Maotianshan Shale, they include H. ercaiensis (Chen et al. 2004e), Leanchoilia illecebrosa (Hou 1987), Jianfengia multisegmentalis (Hou 1987), T. longicaudata (Luo et al. 1999), and F. foliosa (Hou and Bergström 1997). All the non-anomalocaridid procheliceratids have a similar five-segmented head, covered by a cephalic shield and bearing ventral compound eyes in the visual segment, a pair of anteroventral and anteriorly pointing prochelicerae in the second segment, and three postoral segments with biramous appendages, which are similar to one another and are very similar to the trunk appendages. The trunks of all non-anomalocaridid procheliceratids are generally similar, having relatively short tergopleurae with various number of segments: 13 in H. ercaiensis and T. longicaudata, 12 in L. illecebrosa, 20 in Fortiforceps, and 22 in J. multisegmentalis. The shape of the tail end varies, being lanceolate and ringed with short spines in L. illecebrosa but fan-like in J. multisegmentalis. The post-oral appendages are all biramous and morphologically homologous. However, their endopods vary in design from the euarthropod type in H. ercaiensis to a tubular, multisegmented design, with various numbers of segments (about 9 in L. illecebrosa, more than 10 in T. longicaudata, and 15 in F. foliosa).

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Fig. 93 Naraoia spinosa from the Early Cambrian Maotianshan Shale. (a) enrolled preservation with head parallel to bedding plane; (b) anterior portion of body, showing ramifying diverticulae and a laterally extended left antenna; (c) dorsal view of a

nearly complete specimen showing 3D diverticulae and gut; (d) dorsal view of a bent body. Scale bars = 0.5 cm (a, d), 1 cm (b), and 0.2 cm (c)

Among the prochelicerates, H. ercaiensis is extremely interesting in terms of the morphological gap in the chelicerae of the Cambrian “great appendage” arthropods and the living chelicerates. The animal, about 38 mm long, has a pair of prominent, stout prochelicerae accounting for slightly more than one-fourth of its body length (Figs. 97 and 98). The raptorial prochelicera is a proximal arm composed of two segments. The arm is oriented anteroventrally and then bends dorsally at the joint between the segments. The distal claw has three segments and its very prominent proximal segment is drawn out dorsodistally into a stout, slightly curved spine (fixed spine). The next segment is smaller and rounded, and articulates against the proximal claw segment; a dorsodistally oriented,

fixed spine, because of its articulation against the basal segment, can swing against the proximal spine. The last segment, forming the widened base of its spine, is slightly curved against the second spine, acting as a movable finger, swinging against the fixed spine below. The spines in the claw can move apart or close against each other (Chen et al. 2004e). L. illecebrosa (Figs. 99 and 100) is a small (1–3 cm long), commonly occurring arthropod in the Maotianshan Shale. The head has a narrow front margin, with two pairs of small stalked eyes, a short subquadrate hypostome, and a pair of prochelicerae on the lateral surfaces of the hypostome, extending anteriorly. Each prochelicera comprises a two-segmented arm and a four-segmented claw. The segments in the claw are

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Fig. 94 Restoration of Early Cambrian Earcaia minuscule (from Chen 2004)

relatively wide, whereas the subsequent three segments become more slender, and each has an extremely long, filamentous spine, almost the length of the body or longer. These spines can be positioned close together or wider apart (Hou and Bergström 1997). J. multisegmentalis (Figs. 101 and 102) is a rare arthropod, 2 cm long with an elongated body. The head is small and sub-oval, with a pair of stalked eyes and a pair of prochelicerae, with a similar number of segments to those in the head of L. illecebrosa; the arm is longer. The claw has four, slightly more regular, annular segments and straight spines. The trunk consists of 22 segments; the tail is long with a terminal spine. T. longicaudata (Figs. 103 and 104) occurs only in Haikou. It is 2–4 cm long, with an elongated body, small head, slender trunk, and flat tail spine, drawn out from the posterior end of the trunk. The head shield is sub-quadrate in outline, with a separate visual segment jointed to its posterior head shield. It has a pair of lateral eyes situated on the visual segment. The prochelicerae are relatively large, comprising a twosegmented arm and a four-segmented claw. Each of the claw segments is drawn out to form a short spine.

Fig. 95 Earcaia minuscule from the Early Cambrian Moatianshan Shale showing dorsal view of a nearly complete specimen (holotype). Scale bar = 0.5 mm

There are possibly three pairs of post-oral biramous appendages. The trunk has 13 segments, each with a pair of biramous appendages. F. foliosa (Figs. 105 and 106) is a rarely occurring arthropod. It is about 4 cm long, with a slender body comprising a small head, an elongated segmented trunk, and a telson. The head is covered by an oval head shield, and has a pair of stalked eyes and a pair of prochelicerae. The prochelicerae are relatively stout, and consist of a two-segmented arm and a foursegmented claw. The trunk has 20 segments, each with a pair of biramous appendages, each with a flap-shaped exopod and a tubiform endopod, consisting of 15 segments. The conspicuous telson consists of a pair of tubular uropods and a tail spine. Isoxys is a bivalved arthropod distributed worldwide in the Cambrian and occurring commonly in the Lower Cambrian Maotianshan Shale (Fig. 107a–e). It is predominantly represented by empty bivalved carapaces, with two prominent spines of various lengths

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Fig. 96 Earcaia minuscule from the Early Cambrian Moatianshan Shale showing eyes (a, b), 1st pair (a–c) and 2nd pair (c, d) of antennae, multisegmented endopods (a), and uropods (a, b). Scale bar = 500 μm

protruding both anteriorly and posteriorly. The dorsal outline is usually straight, but a few are weakly convex. The carapace has no articulated hinge, and possibly represents a giant head shield derived from the tergite in the second head segment. The soft parts of Isoxys are rarely preserved and are known only from the Lower Cambrian Maotianshan Shale (Chen 2004) and Middle Cambrian Burgess Shale (GarciaBellido et al. 2009). They have an elongated body, covered largely by carapace. The head is presumably short and two segmented, and the first segment carries a pair of large stalked eyes. The appendages on the second head segment were thought to have a regular antennal design, but surprisingly, the Middle Cambrian species, Isoxys acutangulus, documents the presence

of “great appendage”-like structures suggesting that Isoxys is a member of the Prochelicerata. Based on the specimens from the Lower Cambrian Maotianshan Shale, the trunk of Isoxys has numerous (at least 14) segments. Each segment carries a pair of biramous appendages. The endopods are tubular, with numerous segments (approximately 14).

Affinity The affinity of the prochelicerates and the Euchelicerata is confirmed by the common cheliceralike structures in the antennal segment (Fig. 108). The chelicerae are a “chelicerate-only” character,

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Fig. 97 Restoration of Haikoucaris ercaiensis

Fig. 98 Haikoucaris ercaiensis from the Early Cambrian Maotianshan Shale. (a and b) counterparts of holotype

homologous to the antennae in non-chelicerate arthropods. They are characterized by a type of bipartite design, with a proximal arm and a spine-bearing distal claw. In extant Euchelicerata, the chelicerae tend to

be reduced in size or totally lost. The four-segmented chelicera is interpreted as the ground state in the eucheliceratid chelicerae. Both the arm and claw have two segments, but the arm of most euchelicerates has

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . . Fig. 99 Leanchoilia superlata from the Early Cambrian Maotianshan Shale. (a) restoration; (b, c) side view of nearly complete specimens showing 4-segmented claw with three filamentous spines. Scale bar = 0.5 cm

Fig. 100 Leanchoilia superlata from the Early Cambrian Maotianshan Shale. (a) side view of a specimen; (b) ventral view of a specimen, showing four attachment marks of stalked eyes. Scale bar = 1 cm

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The Anomalocaridids: Cambrian Monsters

Fig. 101 Restoration of Jianfengia multisegmentalis

only a single segment through secondary degeneration. The two-segmented claw is a pincer-like structure, with the spine from the first segment acting as the “fixed finger” and the curved conical spine of the terminal segment as the “movable finger”, which can be moved against the “fixed finger” to grasp and crush food. The chelicerae of Haikoucaris differ from both those of the extant euchelicerates and from the prochelicerae of the Cambrian and other non-anomalocaridid prochelicerates in having one more and one less “finger” in the claw, respectively. The difference between the chelicera and prochelicera is phylogenetically significant, suggesting that the euchelicerate chelicera evolved through stepwise reductions in both the size and number of the segments in the claw, from a four-segmented claw through an intermediate state, such as the a three-segmented claw exemplified in Haikoucaris.

The anomalocaridids are a group of early giant predators that shared a single pair of pre-oral “great appendages” (Hou et al. 1999). Their fossils are recorded in the Lower to Middle Cambrian from China, Canada, USA, Poland, and Australia. They were the largest of the Cambrian animals, reaching a maximal length of 2 m, and died out after the Middle Cambrian. The animals are characterized by both a single pair of large, pre-oral raptorial “great appendages” and a large rounded mouth, armed with a ring or several rings of hard, sharp teeth. These pre-oral limb-like appendages are bipartite, resembling those in the other “great appendage” animals. Both are included within the taxon designated Prochelicerata by Chen et al. (Chen et al. 2004e; Chen 2004, 2009). The “great appendages” of the anomalocaridids resemble the prochelicerae of the non-anomalocaridid procheliceratids, with which they share a bipartite design (a distal claw and an arm) and a four-segmented claw. However, the arm in the anomalocaridids is larger and contains more segments, except in Parapeytoia yunnanensis (Hou et al. 1995; Chen 2004), which has a single arm. It was widely believed that the anomalocaridids used these giant “great appendages” to grasp

Fig. 102 Jianfengia multisegmentalis from the Early Cambrian Maotianshan Shale. A and B, counterparts of holotype. Scale bar = 1 cm

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

Fig. 103 Restoration of Early Cambrian Tanglangia longicaudata

their prey and bring it to their mouths. Our observation casts doubt on the argument because the “great appendages” cannot either grasp prey or bend to bring the captured prey to the animal’s mouth. The large rounded mouth armed with numerous teeth is an “anomalocaridid-only” character. The mouth, unlike those of other arthropods, faces ventrally. The teeth are arranged in a circle and those in the outer ring are attached to the margin of the mouth and those in the inner rings to the wall of the oesophagus. The teeth are flat, with a wider proximal end and a serrated, free distal end. The up-and-down motion of the distal free ends of the teeth changes the size of the mouth aperture from maximal to minimal, to capture, crush, and release the prey into the oesophagus. The mouth cannot be closed entirely but presents a relatively large, rectangular aperture, even in its maximally closed state, an indication that the animal could not feed on small prey. The ringed teeth, like cutting nippers, could easily crack relatively large, exoskeleton-protected prey by moving the free distal end from a lower to a horizontal position. In addition to the outer ring, some anomalocaridids have several rings of teeth in their oesophagi. The oesophageal teeth are arranged in the same way as in the outer ring but they become smaller with increasing depth within the

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oesophageal cavity. The motion of the teeth not only cracks and processes the prey into pieces, but pulls the prey deeper into the oesophageal cavity. Anomalocaridids have stalked compound eyes. Their tails have two long, caudal bars and several fin-like structures on the sides of the caudal bars, to maintain their balance when swimming at high speed. They represent the top predators of Cambrian times. It was thought that the anomalocaridids hunted trilobites. However, the undigested residues among the large coprite fossils rarely contain trilobite exoskeletal fragments but predominantly consist of the carapaces of bivalved arthropods related to Chuandianella (a sister group Waptia from the Burgess Shale). The anomalocaridids are truly gigantic creatures for the Cambrian. Based the size of the great appendage and the mouth, the maximal size of the complete animal reaches lengths of 60 cm in Anomalocaris to a staggering 2 m in Parapeytoia. The anomalocaridids are also extremely agile compared with many other sea-dwelling creatures of the time. The animal is segmented and the body has 11 pairs of laterally extended flap-like structures, possibly homologous to exopods. The body probably moved in a wave-like manner, similar to that of present-day rays, allowing it to move at great speed or to “hover” silently (Chen et al. 2007c). Three different species of anomalocaridids are known from the Lower Cambrian Maotianshan Shale: Anomalocaris saron (Chen et al. 1994; Briggs 1994; Hou et al. 1995), P. yunnanensis (Hou et al. 1995), and Amplectobelua symbrachiata (Chen et al. 1994; Hou et al. 1995). A. saron (Fig. 109) is the smallest anomalocaridid, with a maximum length of 60 cm. A completely preserved specimen shows a streamlined

Fig. 104 Tanglangia longicaudata from the Early Cambrian Maotianshan shale showing elongate spine (a, c), multisegmented endopods (b) and prochelicerae (d). Scale bars = 1 cm (a–c) and 0.5 cm (d)

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body with its maximum width one-third from the anterior and a telson consisting of paired, fin-like tail fans and two fine, elongated caudal furca, providing efficient balance while swimming (Chen et al. 1994; Chen 2004). The mouth is ringed with 32 rounded, evenly arranged teeth, but probably no pharyngeal teeth. The trunk has 11 pairs of laterally extended flaps, but no limbs. The great appendages are composed of a large 11-segmented arm and a small 4-segmented claw. A. symbrachiata (Fig. 110) is larger than A. saron, with a maximum length of about 1 m (Chen 2004). Its “great appendage” is similar to that of A. saron but the spines in the proximal fourth segment are much larger. In contrast to A. saron, the front of the body in A. symbrachiata (Fig. 111) is much wider and the eyes lie laterally on the head, rather than in a frontal position. P. yunnanensis has a maximum length of 2 m and is the largest of the anomalocaridids. In contrast to the two other anomalocaridids, the formidable mouth of P. yunnanensis is not only gigantic (25 cm in diameter) but is armed with a ring of teeth on the mouth and numerous rings of teeth within the pharynx (Fig. 112). The great appendages are similar to those of other non-anomalocaridid prochelicerids but relatively shorter, composed of a large one-segmented arm and a four-segmented claw (Fig. 113a, b). Each segment of the claw carries blade-shaped spine. The trunk limbs in P. yunnanensis resemble those in the

Fig. 106 Fortiforceps foliosa from the Early Cambrian Maotianshan Shale. (a and b) counterparts of a nearly complete specimen. Scale bar = 1 cm

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Fig. 105 Restoration of Fortiforceps foliosa

euarthropods in being bipartite, with a huge basipod and a seven-segmented distal limb (Fig. 113c, Hou et al. 1999, 2004). The anomalocaridids were extremely agile. Like present-day rays, the flexible lateral flaps along their bodies could probably be moved in a wave-like formation, allowing the animals to move at great speeds or glide smoothly through the water to approach their prey silently (Chen et al. 2007c). A long-standing view holds that the anomalocaridids fed on hard-bodied animals, including trilobites (Nedin 1999). Some Cambrian trilobites have been found with round or W-shaped “bite” marks, matching the shape of the mouthparts of Anomalocaris. Stronger evidence that the anomalocaridids consumed trilobites is provided by fossilized faecal pellets that contain trilobite parts. However, studies of large faecal pellets from the Maotianshan Shale (Vannier and Chen 2005) have shown that the undigested particles within the faecal pellets (Fig. 114b, c) predominantly contain

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

Fig. 107 Isoxys from the Early Cambrian Maotianshan Shale. (a) Isoxys auritus showing polygonal structure on surface of carapace; (b) a newly molted Isoxys showing multisegmented

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limbs; (c) Isoxys paradoxus showing an elongated rear projection of the carapace; (d–e) Isoxys curvirostratus showing stalked eye. Scale bar = 1 cm (a–d) and 0.2 cm (e)

Fig. 108 Scenario for the evolutionary origin of the Chelicerata

the carapaces of either Chuandienella (a close relative of Waptia of the Burgess Shale; Fig. 114a) or microscopic bradoriids (Fig. 80b). In addition to arthropod carapaces, some faecal pellets predominantly contain exoskeletons related to hyoliths (Chen 2004). Because the mouth in the anomalocaridid cannot close fully and a large central aperture remains in the maximally closed state, we infer that the anomalocaridids could

not fed on microscopic arthropods such as bradoriids. Furthermore, hyolithids were epibenthic organisms, so it is unlikely that these hyolithid faecal pellets were produced by anomalocaridids. The producers of these giant faecal pellets containing bradoriids and hyolithids remain a mystery. Thus, Chuandienella and some other arthropods were the main diet of the anomalocaridids during the Early Cambrian.

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The Evolutionary Scenario of the Panarthropods

Fig. 109 A nearly complete Anomalocaris saron from the Early Cambrian Maotianshan Shale. Scale bar = 2 cm

The Arthropoda represents a vast assemblage of segmented animals with exoskeletons and jointed appendages. Their tremendous adaptive diversity has allowed them to survive in many and various environments with tremendous diversification. They are the most successful animal phylum on our planet in terms of population size and species diversity, accounting for about 80% of all known animal species. The evolutionary origins of this group are hotly debated (e.g., Wang and Chen 2004). Because living arthropods are highly modified, belonging to the crown lineages of the euarthropods, and because the fossil record is incomplete, the large gap in the early evolutionary history of the arthropods has made discussion of the arthropod origins highly speculative and poorly grounded in evidence. New fossil discoveries, especially in the Lower Cambrian Maotianshan Shale, in the past two decades have profoundly changed our understanding of the origins and evolution of the arthropods. The fossils, including the worm-like ancestors, the first arthropods (or “proarthropods”) with unjointed limbs, the intermediate forms between the proarthropods and

Fig. 110 Two nearly complete Amplectobelua symbrachiata from the Early Cambrian Maotianshan shale. Scale bars = 2 cm (a) and 3 cm (b)

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Fig. 111 Formidable “great appendages” of Amplectobelua symbrachiata from the Early Cambrian Maotianshan shale. Scale bar = 1 cm

Fig. 112 Formidable mouth apparatus of Parapeytoia yunnanensis from the Early Cambrian Maotianshan Shale. Scale bar = 1 cm

euarthropods, the stem-lineage euarthropods ancestral to the Mandibulata, and the stem-lineage Chelicerata, shed new light on the mysterious history of the origin and early evolution of the arthropods. They provide evidence of a grand scenario, with a complex texture

of the step-wise evolution that progressed in multiple parallel lines, involving cephalization, sclerotization, arthropozation, arthropodization, segmentation, and tagmatization.

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Fig. 113 “Great appendages” (a, b) and limbs (c) in Parapeytoia yunnanensis from the Early Cambrian Maotianshan Shale. Scale bar = 1 cm

Fig. 114 Chuandianella ovata and coprolites from the Early Cambrian Maotianshan Shale. (a) Chuandianella ovata; (b, c) giant coprolites with undigested carapaces similar to those of Chuandianella ovata. Scale bar = 1 cm

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Cephalization: Origin of the Arthropod Head and the Evolution of Arthropod Head Segmentation The head accommodates the sensorial and feeding organs externally and the brain, oesophagus, and midgut internally. Cephalization lies at the core of arthropod evolution. Fossils delineate the step-wise evolution of the arthropods in multiple parallel lines, including head segmentation, morphological and functional specialization, and the modification of the head appendages for sensory and feeding roles. The head is segmented externally, the segmentation providing evidence with which to trace the pathway of its evolutionary changes. However, the segmental homology and segmental identity with the extant arthropod head have been obscured by the fusion, modification, and relocation of these segments in some taxa, especially in the insects. Consequently, the head segmentation of the arthropods has been an enduring puzzle. Comparative studies of representative fossils from the Lower Cambrian Maotianshan Shale at different evolutionary stages have contributed to a new understanding of the evolutionary origin of the arthropod head. Cephalization is rooted in the early history of the panarthropods. The worm-like animals (tardipolypods) in the Maotianshan Shale document the development of the panarthropod head and its differentiation into three different patterns, the non-segmented head, the one-segmented head, and the two-segmented head, although these early heads are scarcely distinguishable from the trunk (Fig. 115-1–3). It is unclear which of the three heads represents the ground plan of the panarthropod head. The head is the result of an early tagmosis event, a simple process that organized the segments into an anterior head and a posterior trunk. Tagmosis coevolved with sclerotization. Interestingly, the first sclerotization occurred in the domain related only to the trunk appendages. The head represents the front part, anterior to the anterior sclerites. The head appendages are also usually more laterally situated, more slender, and longer than those on the trunk. The least complicated proarthropod head represents the ground plan of the arthropod head. It is short, consisting of two segments corresponding to the visual and antennal segments of the anterior head region

Fig. 115 States of the head in the stem lineage of Panarthropoda with non-segmented head (1), one-segmented head (2) and two-segmented head (3); Proarthropoda (4) with two-segmented head; transitional forms (5) from Proarthropoda and Euarthropoda; stem-lineage euarthropods (6); stem lineage of the Chelicerata (7); Euchelicerata (8); stem lineage of the Mandibulata (9) and Eucrustacea (10)

in the euarthropod syncephalon (Fig. 115-4). The two-segmented primitive head is known as the “procephalon”. The visual segment has a pair of stalked eyes and the antennal segment has a pair of short antennae. Although the head in the first arthropods had the same number of segments as observed in the wormlike ancestors (Cardiodictyon+Hallucigenia clade), the morphological gap in the heads of the worm-like ancestors and the first arthropods is very great. The cephalization that occurred in the transition from the worm-like ancestor to the arthropods was a great evolutionary leap, marked by multiple parallel changes that included the relocation of the terminal mouth to a new position (below the second segment) with the backward folding of the visual segment, and the

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modification and functional specialization of the head appendages into visual and mechano-chemosensory organs. The ground plan of the head in the euarthropods is characterized by a five-segmented syncephalic head (Fig. 115-5 and 6). During the proarthropod-toeuarthropod transition, cephalization was marked by the formation of the five-segmented head with a bipartite design, whose two anterior segments were virtually identical to the head in the proarthropods, known as the “procephalon” or “pro-head”. The posterior three segments, which were apparently recruited from the anterior trunk, form a novel structure, here referred to as the “meta-head”. The appendages in the metahead are biramous and morphologically resemble those in the trunk in the stem-lineage euarthropods. Why the meta-head in the early euarthropods was three segmented, rather than one, two, or four segmented, remains a puzzle. The cephalization that progressed towards the Cheliceratida was marked by the modification of the antennae into chelicerae for feeding (Fig. 115-7 and 8). However, the evolutionary novelty in the origination of the Mandibulata was the modification of the metahead appendages into feeding organs. In addition to the morphological and functional modifications to the head appendages, cephalization was also marked by a second round of rearward expansion to form the foursegmented meta-head in the Mandibulata (Fig. 115– 9 and 10) and the five-segmented meta-head in the Euchelicerata. The fossil evidence shows that the evolutionary origin of the Mandibulata head progressed in two separate events. Ercaia represents the first event, which was marked by the modification of the first pair of appendages in the meta-head into antennae-like structures. The second event occurred shortly after the first event and is represented in the first eucrustaceans (Zhang et al. 2007; Siveter et al. 2001). This event involved the modification of the second to fourth pairs of appendages into feeding organs (designated the mandible and maxilla 1 and 2, respectively). The Crustacea is the stem group of the Mandibulata, and the insects and myriapods evolved from the crustaceans. Cephalization that occurred during the evolutionary transition from the crustacean-like ancestor to the insects and myriapods was marked by the modification of the second antenna-bearing segment into the

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intercalary segment, a segment that has long been considered to be limbless. Because the head of the Insecta has been highly modified and some of the head structures have been displaced, the segmentation of the head and the identity of the head structures have been controversial. The labrum (or upper lip), a plate-like process anterior to the mouth field, is the most unexpected structure. It led some authors to speculate that the anteriormost part of the head is of non-segmental origin. The term “acron” was introduced to represent the non-segmental region. The acron includes the labrum only, according to some authors (Snodgrass 1935; Rempel 1975; Scholtz 2001), but it has been interpreted as representing a fused anterior part of the head that includes the labrum, eye, and protocerebrum by others (Brusca and Brusca 2002). Based on the later interpretation, the pre-oral part of the head is composed either of a non-segmental part and two segments or of a non-segmental part and one segment. The appendicular origin of the labrum is well supported by both embryological (Eastham 1930; Butt 1960; Rempel 1975) and molecular developmental studies (Schmidt-Ott and Technau 1992). Whether the labrum represents the anteriormost segment or alternatively the intercalary segment and whether the insect head has six or seven segments are ongoing debates. Molecular and neural studies (Boyan et al. 2002; Popadic et al. 1998) have proposed that the labrum is the fused paired appendages of the intercalary segment, so that the modification of the second antennae into a feeding organ was one of the key evolutionary novelties in the origin of the Tracheata (Hexapoda+Myriapoda). The cephalization in the Chelicerata lineage is marked by the modification of the antennal appendages into feeding organs, known as the “chelicerae”. The evolution of the chelicerae progressed in multiple steps. The anomalocaridid type of “great appendages” probably represents the ground plan of the chelicerae, characterized by large, multisegmented arms and foursegmented claws. The extant chelicerae evolved from the ground plan through two transitional steps, a design with a four-segmented claw and a two-segmented arm (in most stem-lineage chelicerates) and a design with a three-segmented claw and a two-segmented arm (in Haikoucaris). The meta-head in the living Chelicerata has five segments. In addition to the modification of the antennae into feeding organs, the cephalization in the

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

Chelicerata had evolved with a second round of rearward expansion in the meta-head. A seven-segmented mode characterizes the ground plan of the euchelicerates and suggests that the second expansion event occurred in the Silurian, when the first-known sevensegmented chelicerate head is reported in the fossil record (Sutton et al. 2002).

Tagmatization and the Origin of the Molecular Axial Bipartite Domains Head and trunk bipartization characterizes the tagmatization that occurred during the transition from the worm-like ancestor to the arthropods. However, the head/trunk bipartite design of the body was already clearly recognizable in the worm-like ancestors (as exemplified by the Cardiodictyon+Hallucigenia clade). The trunk in the proarthropod Fuxianfuia displays a clear bipartite pattern, with a limb-bearing thorax and limbless abdomen, suggesting that the reorganization of the trunk segments into bipartite regions occurred in the proarthropod evolutionary stage. The fusion of some or all of the thoracic segments with the head to form a cephalothorax occurred in many crown-lineage chelicerates. Molecular and genetic research has confirmed that all bilaterian animals, including the arthropods and humans, have a common genetic mechanism, with the Hox cluster genes patterning the anterioposterior axis along the main axis of the body, except in its anteriormost part, which is outside the Hox gene expression domain. Recently, it has become clear that the anterior margin of the Hox gene domain is conserved among different extant arthropod groups and lies at a position close to the border between the anterior and posterior developing head of the extant arthropods, but is not tied to the morphological boundary between the head and the trunk (Fig. 115-5–10). The anterior head, outside the Hox gene expression domain, is comprised of two segments, the anterior ocular and the posterior antennal segments, innervated by the protocerebrum and the deutocerebrum, respectively. The otd/otx genes are both involved in the patterning of the anterior head and the rostral brain. The boundary of the two developmental subdivisions of the body (the anterior otd/otx-specified and posterior Hox-specified region) is conserved not only across the different extant arthropod groups but also throughout the different

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bilaterian animals. It is difficult to understand why the molecular boundary does not match the morphological head–trunk boundary. Fossils may provide the answer. The morphological boundary of the head and trunk is not conservative. The trunk in the proarthropods represents the post-antennal part of the body and the boundary between the head and trunk well matches the molecular boundary between the Hox gene expression region anteriorly and the ems/otd gene expression region posteriorly. The arthropod head has a tendency to expand with the posterior displacement of the morphological head–trunk boundary, so the molecular boundary has a more anterior position than the morphological boundary. Expansion characterizes the evolution of the arthropod head with the gain of a head segment when the head shifted posteriorly beyond the border. The original position of the head–trunk boundary in the arthropods, as exemplified by the proarthropods, was situated at the rear margin of the antennal segment, at a much more anterior position than that in the extant arthropods. The implication is that the molecular boundary between the anterior otd/otx domain and the posterior Hox domain is highly conservative and ancient and that its relationship to head segmentation has not changed since its first establishment in the earliest arthropods. The ancient head–trunk boundary has vanished morphologically and has virtually left no distinct morphological mark, except in a few extant arthropod species. For instance, in developing Drosophila, a transient structure known as the “cephalic furrow” may represent a relic of the ancient head–trunk boundary. The cephalic furrow lies at the junction of the patterning systems that define the procephalic and segmental germs (Costa et al. 1993; Vincent et al. 1997) and the cells in the transient structure all unfold back onto the surface of the embryo, contributing to the ectoderm in later stages (Costa et al. 1993). The cephalic furrow is interpreted as an early organizer region analogous to the midbrain–hindbrain border (MHB) in the vertebrates (Ball-Cuif and Wassef 1995; Joyner 1996). The antennal segment forms a posterior part of the early arthropod head and bears a very large and posteriorly extended cephalic shield. The large and posteriorly extended tergite of the antennal segment is characteristic of the first arthropod head, and a similar structure also reappears in some extant crustaceans (Casanova et al. 2002).

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“Arthropoda”, from the Greek word for “jointed feet”, refers to those organisms with jointed limbs. Arthropodization is the development of segmented

and jointed trunk limbs and is thought to have been a novelty of the arthropods. The first arthropods, exemplified by the proarthropods, had a segmented and jointed body, but soft-bodied and unjointed trunk limbs. This indicates that arthropozation and arthropodization were not synchronous and that arthropozation predated arthropodization. The diverse arthropod fauna, together with their worm-like ancestors, provides a unique window through which to establish the evolutionary development of the arthropod appendages. It is suggested that the arthropods derived from a worm-like ancestor that closely resembled the “Hallucigenia+Cardiodictyon” clade. The presumed worm-like ancestor had a simple, elongated body divided into serial segments. Each segment had a pair of soft, unjointed, uniramous appendages, with a single-tube form. These appendages had multiple annulations and lacked an intrinsic musculature. The preservation of a central cavity in some appendages suggests that these limbs were hydraulic. The appendages were paired and undifferentiated, except for the more dorsal, slender, head appendages. The evolutionary origin of the Arthropoda was marked by the transformation of the head appendages into sensorial organs, and by the transformation of the uniramous trunk appendages (Fig. 116-1) into biramous appendages (Fig. 116-2). The jointed limbs arose during the transition from the proarthropods to the euarthropods. The first jointed limbs (Fig. 116-3) were tubular, tapered slowly, and were composed of 17–20 regular annulus, connected to one another by pivot joints (Hou et al. 1999, 2004). The presence of a pivot joint suggests the presence of

Fig. 116 Evolutionary scenarios in trunk limbs of Panarthopoda. (1) unjointed monoramous limb; (2) biramous appendages with unjointed exopod; (3) biramous appendages with multisegmented exopod; (4) biramous appendages with

multisegmented, bipartite exopod; (5) biramous appendages with multisegmented, bipartite exopod but fewer segments in the proximal portion; (6) biramous appendages with bipartite exopod

Sclerotization and Arthropozation The ground state in the exoskeleton of the panarthropods is characterized by a soft and flexible cuticle. The hardening of the cuticle to form hard sclerites is accomplished by sclerotization, which is deeply rooted at the base of panarthropod evolution. As exemplified by the tardipolypodians in the Maotianshan Shale, the early sclerotization event was restricted to the trunk, forming paired, morphologically diverse sclerites dorsal to the trunk appendages. Arthropozation characterizes the arthropods and represents a significant event during the transition from the worm-like ancestors to the arthropods. Arthropozation is characterized by the hardening of the cuticle into separated plates, which are both metamerically arranged and transversely arranged into four parts (a dorsal tergite, a pair of pleurates, and a ventral sternite). These sclerites are connected by soft, flexible cuticle, known as “articular membrane”. Arthropozation is accomplished by the formation of the articular membrane (otherwise known as the “joint”). Early arthropozation was restricted to the head and trunk, as exemplified in the proarthropods of the Maotianshan Shale, and excluded the trunk limbs, which remained soft bodied.

Arthropodization and the Evolution of the Trunk Limb

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intrinsic muscles and that these annuli were true segments. The biramous trunk is a novelty of the arthropods, and the first biramous trunk appendages were characterized by an unjointed endopod and gill-less exopod. The ground plan of the jointed endopod was tubiform and multisegmented. The euarthropod limb has fewer segments (seven or fewer) with strong distal– proximal differentiation, forming a bipartite design: a distal slender part and an expanded basipod. The euarthropod limb developed from the multisegmented tubiform, through intermediate stages. The limb in the intermediate stage is characterized by a bipartite design, with a multisegmented and expanded proximal part (Fig. 116-4, 5). It is proposed that the evolution of the euarthropod limb progressed in two separate steps: distal–proximal axial differentiation and the fusion of the multisegmented, expanded part into a single basipod. Arthropodization occurred during the evolutionary transition from the proarthropods to the euarthropods and involved the formation of segmented and jointed trunk limbs. Euarthropoda has been defined as monophyletic, both in terms of its five-segmented head and its post-antennal limb design (Waloszek 1999; Maas and Waloszek 2001). The authors propose that the post-antennal limb in Euarthropoda consists of a rigid, anterioposterior-compressed proximal part (the basipod) and a seven-segmented endopod (Fig. 116-6). However, the bipartite design of this limb along its main axis does not always appear in the stem groups of the Euarthropoda. In numerous species of the distally related stem groups of the Euarthropoda (Canadapsis, Isoxus, Ercaia, Primicaris, Tanglangia, Fortiforceps, Leachoilia, Saperion, and the bradoriids), the postantennal limbs do not display the expected bipartite design, but a simple, tubular form with slight differentiation along the main axis and 9–15 segments. This implies that the bipartite limb design is not monophyletic. The anterioposterior-compressed basipod with its expanded and serrated inner edge was probably associated with feeding activity, breaking large food items into pieces, and with the anterior transportation of food to the mouth. The origin of the expanded basipod with its serrated inner edge is a pivotal event in the change from microphagous to macrophagous feeding behaviour. Proximodistal specification is the basis of the evolutionary change in limb design. This change drove the

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limb towards a progressive increase in its differentiation along the main axis, in a stepwise manner from the simple, multisegmented, tubular limb to the bipartite design, via intermediate steps. The limb design during these intermediate steps is exemplified by Canadaspis (Fig. 116-4) and Saperion (Fig. 116-5), which display clear proximodistal domain differentiation, with an expanded, multisegmented, proximal domain. The transformation of the intermediate form into a limb with two functional domains (Fig. 116-6) probably resulted from the fusion of the multisegmented, proximal domain into a single-segmented proximal domain, known as the “basipod”. Both the limbs and antennae of extant arthropods express the same proximodistal axis patterning genes during their development, including Distal-less (Dll), dachshund (dac), and homothorax (hth) (Dong et al. 2001). The products of these patterning genes either act together or act in mutually exclusive ways. The mutually exclusive regulatory gene products allow the development of sharp boundaries between domains. Both the limb and antennae, as exemplified in the proarthropods, have a simple tubular shape, with the least proximodistal differentiation in the early arthropods. This mutually exclusive genetic regulatory interaction underlying limb or antennae patterning had not yet appeared in the early arthropods. The presence of bipartite antennae, known as “prochelicerae”, in the stem groups of the Chelicerata and bipartite limbs among the stem groups of the Euarthropoda implies that this mutually exclusive regulatory interaction of the patterning gene products evolved to define the sharp boundary between these domains in both the antennae and limbs. The differentiation of the head and trunk appendages suggests that two axial molecular domains, such as the otd/ems and Hox gene domains, had been established at the very beginning of arthropod evolutionary history. The otd/ems genes in the head region were selectively expressed to modify the simple, tubular head appendages into stalked compound eyes and antennae, respectively. The Hox genes were selectively expressed in the trunk region and were responsible for biramous appendage development. The exopod is a novel structure in the arthropods and its flap-like form represents an extended pouch of the body wall, which resembles the insect wing in its general morphology. Its evolution was presumably regulated by a gene cassette similar

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to that involved in the developing wings of extant insects. The speciation of the appendages in arthropods evolved roughly in an anterioposterior direction along the body axis during arthropod evolution. The first event of appendage speciation was the transformation of the first appendage into a visual organ, the eye stalk. The following event was the independent modification of the short limb-like structure in the second segment into a whip-like sensorial or grasping organ, at a transitional stage from the proarthropods to the euarthropods. The speciation of the post-antennal appendages in the head of the Mandibulata involved three separate events. The earliest event, exemplified by Ercaia, was the transformation of the first post-oral appendage into the second antenna. The recent discovery of Early Cambrian eucrustaceans from both north-eastern Yunnan, China (Zhang et al. 2007), and Shropshire, England (Siveter et al. 2001) suggests that the origin of the gnathal appendages followed soon after the origin of the second antenna. The gnathal appendages (called the mandible, maxilla 1, and maxilla 2) are feeding organs, comprising structures modified from the second to fourth post-antennal appendages. The appendages also differentiated in a caudalto-anterior direction. A loss of appendages characterizes this anterior-directed differentiation, linked to the process of abdominalization (Boxshell 2004). Abdominalization may have occurred repeatedly in the evolutionary history of the arthropods. Fuxianhuia is a fossil representative of the earliest abdominalization event at the very beginning of arthropod evolutionary history.

Centralization of the Nervous System The developmental regulatory genes of the orthodenticle (otd/otx) gene family and the Hox gene family not only act in the specification of the embryonic, anterioposterior body axis but are also involved in brain development in both insects and mammals. The otd/otx genes are involved in the development of the rostral part of the brain and the Hox genes in its caudal development. The molecular and genetic similarities in the brain development of insects and mammals have led some researchers to draw the conclusion that a tripartite organization of the embryonic brain was already

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established in the last common urbilaterian ancestor of the protostomes and deuterostomes (Hirth et al. 2003). Other studies refute the early origin of the tripartite brain organization (Chen 2008, 2009). The arthropods have recognizable head segments, and these and the corresponding appendages appear closely related to brain regionalization. The relationship between the head segment and brain regionalization is consistent across distally related groups of extant arthropods implying that the relationship is very highly conservative and ancient, and established at the first appearance of the arthropods. The visual system in the ocular segment is an important component of the protocerebrum, and the olfactory centres of the antennal segment are the major components of the deutocerebrum. All these systems and the related protocerebrum and deutocerebrum were already present in the first arthropods, as exemplified by the Lower Cambrian proarthropods. The caudal brain comprises the posterior suboesophageal ganglion and three sub-oesophageal neuromeres; these are connected to the second antennal segment and the three gnathal segments of the posterior head, respectively. The caudal brain, connected to the post-antennal head segments, apparently had not developed in the first arthropods, suggesting the caudal brain is a secondarily derived structure probably originating from the modification of the trunk ganglia. In extant insects, the caudal brain (tritocerebrum) is composed of the mandibular, maxillary, and labial neuromeres; these are connected to the feeding organs, including the labrum, mandibular, maxillary, and labial organs. The stem groups of the Euarthropoda had only three post-oral segments and related unspecialized appendages. These post-oral head segments and their related appendages were strikingly homologous to those in the trunk. It is unlikely that the caudal brain had evolved in the early euarthropods.

Grand Evolutionary Scenario Panarthropoda represents a monophyletic taxon that presumably derived from a segmented appendageless worm-like ancestor, as shown in Fig. 117 (Fig. 117-1). The monoramous unjointed trunk limbs were the key novelty in the evolutionary origin of this group. Cephalization and sclerotization occurred within the trunk during the early evolution of the panarthropods and led to the formation of three principal

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Fig. 117 Diagram of phylogenetic kinship of the high ranking clades among the Panarthropoda. (1) common ancestor of Panarthropoda characterized by paired trunk limbs which were monoramous and unjointed; (2) stem-lineage Panarthropoda with non-segmented head; (3) origination of segmented head; (4) stem-lineage Panarthropoda with one-segmented head; (5) origination of two-segmented head; (6) stem-lineage Panarthropoda with two-segmented head; (7) evolutionary origin of the arthropods (with key novelties: relocation of mouth, transformation of 1st pair of head appendages into stalked eyes, 2nd pair of head appendages with antennae, head and trunk arthropodization, and transformation of trunk limbs from monoramous to biramous; (8) the first arthropods (proarthropods); (9) evolution towards euarthropods; (10) evolution towards crown lineage arthropods; (11) evolutionary origin of Chelicerata; (12) stemlineage Chelicerata; (13) Euchelicerata; (14) evolutionary origin of Mandibulata—marked by transformation of the 1st pair of post-oral appendages into 2nd antennae; (15) the Ercaia-like first Manbibulata; (16) evolutionary origin of the Eumandibulata (marked by transformation of the 2nd to 4th post-oral head

appendages into feeding organs); (17) Crustacea representing the stem group of the Eumandibulata; (18) evolutionary origin of Tracheata—marked by transformation of the 2nd antennae into a feeding organ (the labrum), formation of a novel tracheal system and degeneration of the exopods; (19) Myriapoda representing the stem-lineage of the Tracheata; (20) Hexapoda arising from a myriapod-like ancestor, presumed to be through parallel lines of evolutionary change including tagmatization of the trunk leading to formation of a three-segmented thorax and limbless abdomen, origin of water-conservation structures (the spiracle with closing mechanism, excretion of uric acid, and the waxyimpregnated epicuticle), and origin of wings on the thorax; (21) extinct euarthropods characterized by having bipartite post-oral limbs; (22) Naraoiids characterized by having a bipartite body, non-mineralized exoskeleton and absence of eyes; (23) origin of tripartite bodied euarthropods; (24) Trilobita characterized by having a mineralized exoskeleton, sessile dorsal eyes, presence of three axial lobes and tripartite body; (25) Trilobitomorpha by non-mineralized exoskeleton, stalked and ventrally situated eyes

stem lineages characterized by different types of head design: the non-segmented-head group (Fig. 117-2), the one-segmented-head group (Fig. 117-4), and the two-segmented-head group (Fig. 117-6). The phylogenetic relationships among the three different groups are unclear. The non-segmented-head group is presumed to be the primitive one, whereas the twosegmented-head clade represents an advanced group. The arthropods presumably derived from a wormlike ancestor with a two-segmented head (Fig. 117-6) resembling Hallucigenia+Cardiodictyon. The transition from the worm-like ancestor to the arthropods (Fig. 117-7) was an evolutionary leap achieved via numerous synchronous events. These included arthropozation, cephalization, and the transformation of monoramous limbs to biramous limbs. Arthropozation

represents an advanced evolutionary stage of sclerotization, characterized by the presence of a hardened cuticle on both the trunk and head, but not on the limbs. The hard cuticle is divided into plates (sclerites) separated segmentally and transversely, and connected by flexible cuticle known as the articular membrane. Cephalization occurring at the origin of the arthropods was marked by evolutionary novelties such as the relocation of the mouth opening from the anterior terminus to a ventral position at the level of the second segment, and the modification of the head appendages to visual organs, including stalked eyes and antennae. The trunk region was modified by the transformation of the monoramous limbs into biramous limbs. The fossils in the Maotianshan Shale show that the arthropods are a monophyletic taxon, but that the

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euarthropods did not arise from a common ancestor and were probably polyphyletic. The evolution of the arthropods occurred as two parallel processes: arthropodization and cephalization. Living arthropods consist of two principal taxa, the Chelicerata (Fig. 11711) and the Mandibulata (Fig. 117-14), which are deeply rooted among transitional stages between the proarthropods and the euarthropods (Fig. 117-8, 9 and 10). The chelicerae developed from antenna-like structures on the antennal segment and constitute one of the key novelties in the evolutionary origin of the Chelicerata (Fig. 117-11) leading on to the taxa Prochelicerata and Euchelicerata (Fig. 11712, 13). The evolutionary origin of the Mandibulata was marked by the modification of the post-oral head appendages into antenna-like structures, known as the second antennae, as exemplified by Ercaia from the Maotianshan Shale. This animal has a pair of second antennae, but unlike extant Crustacea, its other post-oral head appendages remain similar to the trunk appendages suggesting that the evolution of the Mandibulata proceeded in a step-wise manner towards Promandibulata (e.g. Fig. 117-15). The transformation of the first post-oral head appendage into an antennalike structure occurred earlier than the evolutionary transformation of the post-oral second to fourth head appendages into feeding organs, leading to the origin of the Eucrustacea and Crustacea (Fig. 117-16 and 17). The transformation of the second antennae into a feeding organ, known as the “labrum”, represents one of the important evolutionary novelties leading to the origin of the Tracheata (Fig. 117-18). The origin of the Tracheata was also marked by the innovation of the tracheal system and the degeneration of the exopods. The Tracheata comprises two possibly monophyletic taxa, the Myriapoda (Fig. 117-19) and the Hexapoda (Fig. 117-20). The Myriapoda probably represents a stem group of the Tracheata (Fig. 117-18), with a bipartite body, a head, and an elongated untagmatized trunk containing numerous segments, each bearing a pair of limbs. The tracheal system is at a primitive stage, with spiracles that usually cannot be closed and are not well protected from water loss. The Hexapoda (Fig. 117-20) probably arose from a myriapod-like ancestor, along parallel lines of change, including the following: tagmatization of the trunk leading to the formation of the three-segmented thorax and limbless abdomen; water conservation structures including spiracles with a closure mechanism; the excretion of

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uric acid; a wax-impregnated epicuticle; and wings on the thorax. The bipartite design of the trunk appendages is interpreted as a key criterion in the definition of the Euarthropoda. This bipartite limb evolved in a stepwise way from the jointless annulated limb of the proarthropods, through several intermediate steps (Fig. 117-21). The first evolutionary step was the formation of the limb joints, and the ground plan of the jointed limb is characterized by a slender, multisegmented, jointed limb with little distal–proximal differentiation. The subsequent step was marked by distal–proximal axial differentiation leading to the formation of a slender, multisegmented distal portion and a greatly expanded proximal portion. The bipartite limb with a single, expanded basipod and a multisegmented, slender distal portion, described as the “euarthropod type of limb”, probably arose from a bipartite limb with a multisegmented, expanded proximal portion through the fusion of the segments in the proximal portion. The fossils in the Maotianshan Shale show that the ancestral forms of both the Chelicerata and Mandibulata had slender and multisegmented trunk limbs. The euarthropod type of limb apparently evolved independently in the two taxa. Interestingly, the Trilobita (Fig. 117-24), Trilobitomorpha (Fig. 11725), and Naraoiida (Fig. 117-22), the three distinct groups considered the stem-lineage euarthropods, all have trunk limbs with the typical euarthropod design (Fig. 117-23).

Vetulicolians and Their Affinities Vetulicolians are large Cambrian animals with a tripartite body composed of a simple cone-shaped head, a larger expanded, segmented thorax, and a dorsoventrally flattened abdomen. The mouth and anus open at opposite ends of the body. The thorax is enclosed by an exoskeleton composed of a pair of flexible pleural membranes and dorsal and ventral plates. The exoskeleton is modified to form lateral segmentally arranged gill chambers. These shared features suggest that the vetulicolids are a monophyletic group. They are an extinct group, known in both the Lower Cambrian Maotianshan Shale and the Middle Cambrian Burgess Shale. In the Burgess Shale, they are represented by the highly modified species Banffia constricta (Walcott 1911b; Caron 2006).

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The vetulicolids include Vetulicola cuneata (Hou 1987), Didazoon haoae (Shu et al. 2001b), Yuyuanozoon magnificissimi (Chen et al. 2003a), Heteromorpha confusa (Chen and Zhou 1997; Luo et al. 1999), and Pomatrum ventralis Lu and Hu 1999 (= Xidazoon Shu et al. 1999a) from the Lower Cambrian Maotianshan Shale and B. constricta (Walcott 1911b; Caron 2006) from the Middle Cambrian Burgess Shale. Of these, V. cuneata occurs commonly in the Maotianshan Shale and is characterized by a large, laterally compressed thorax and a dorsoventrally flattened abdomen. The thorax is sub-rectangular in lateral view, with a compressed cross section, and a height twice as great as its width. The thorax has five fused segments, each with a pair of gill-bearing chambers (Figs. 118 and 119). The exoskeleton comprises four plates transversely comparable to the dorsal plate, the pair of lateral flexible pleural membranes, and the ventral plate in Arthropoda. The dorsal and ventral plates are both finned in their median planes and are thick, consisting of a thin, dark outermost layer (Fig. 119d) and a thick, pitted inner layer (Fig. 119a), comparable to the epicuticle and procuticle in the arthropods, respectively. The pitted structure of the inner layer in V. cuneata indicates the presence of microscopic canals. Identical microscopic canals are also present in the inner layer of the arthropod sclerites (Brusca and Brusca 2002). In addition to fine pits, the inner layer also displays a distinct transverse linear structure (Fig. 119a); this may represent the segment boundary. The lateral pleural membranes are thin and flexible, extending across the middle of the thorax for its entire length. They are contractive and usually preserved in the contracted state (Fig. 119a, b, d). Figure 119c shows a fully exposed pleural membrane. Each of the thoracic segments has a pair of pearshaped, gilled chambers with their narrower ends pointing anteriorly (Fig. 120). As in many living

Fig. 118 Reconstruction of Vetulicola cuneata

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crustaceans, the gill chambers are formed by invaginations of the exoskeleton and have a wall with gill filaments lodged on its inner side; probably protecting the fragile gill filaments from damage. Similar gill-bearing branchial chambers occur widely in extant decapod crustaceans. Anterior to the thorax are two pairs of sclerites, possibly protecting the soft-bodied head. The abdomen is limbless, oar-like, and compacted dorsoventrally. It consists of seven jointed segments, each boxed by a dorsal plate, with two narrow lateral pleural joints and a ventral plate, exactly as in the arthropods (Brusca and Brusca 2002). The abdomen, rounded anteriorly and increasingly flattened posteriorly, inserts dorsally into the rear end of the thorax. The segments are equal in length, apart from the terminal one which is semi-circular in shape and much longer than the others. The gut is regularly bead like (Fig. 121), with an anus opening ventrally near the rear end of the last segment (Fig. 119d). P. ventralis is usually 7–10 cm long (20 cm maximum length), with an elongated thorax, consisting of five segments, each rounded in cross section (Fig. 122). Each segment has a pair of gill chambers. The abdomen resembles that of Vetulicola and is subdivided into seven equal segments, except for the last, much longer one. The head is exposed externally, with no protection from anterior sclerites as seen in Vetulicola, and it is small, short, and conic, only 3– 4 mm long and 2 cm in diameter. Its gut is identical to that of Vetulicola, with a bead-like shape. Heteromorphus confusa is soft bodied, usually 3.5– 5 cm long, maximally 6 cm (Fig. 123). It has a small, rounded head protruding anteriorly from the thorax. The thorax is rectangular in side view, laterally flattened, and consists of four segments, each bearing a pair of lateral gill chambers. Like the Middle Cambrian B. constricta, the abdomen has 20 closely arranged segments. The segments are of equal length, except for the last, much longer one; this is semi-circular in outline when viewed from the dorsal surface. The gut is simple and straight, ending ventrally at an anus near the terminal end of the last segment. Y. magnicissimi is a large vetulicolid, about 20 cm long (Fig. 124). A short, rounded head projects anteriorly from the thorax. The thorax is an elongated oval in outline, composed of five segments, each bearing a pair of gill chambers. The abdomen consists of seven segments, probably sub-rounded in cross section.

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Fig. 119 Vetulicola cuneata from the Early Cambrian Maotianshan Shale showing fused segmented structure (a), pitted exoskeleton (a), contracted (a, b, d) and exposed lateral

Fig. 120 Pear-shaped gilled chamber and gills within the chamber in Vetulicola cuneata from the Early Cambrian Maotianshan Shale. Scale bar = 1 cm

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pleural membrane (c), and gilled chambers (a–d) of thorax, and limbless oar-like abdomen with jointed segments. Scale bars = 1 cm (a, b), 2 cm (c) and 3 cm (d)

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Fig. 121 A laterally compacted abdomen of Vetulicola cuneata from the Early Cambrian Maotianshan Shale showing bead-like gut. Scale bar = 1 cm

Affinities The vetulicolids are a monophyletic taxon, sharing a tripartite body comprising a small non-segmented head, a fused segmented thorax with paired gillbearing branchial chambers, and a segmented limbless abdomen. However, the affinities of the vetulicolids are controversial. They are interpreted as arthropods or an arthropod-related animal group (Chen and Zhou 1997; Bergström and Hou 2003; Chen 2004; Briggs et al. 2005; Caron 2006), or as either basal (Shu et al. 2001b) or more derived deuterostomes, probably close to the tunicates (Gee 2001; Lacalli 2002; Aldridge et al. 2007), or even as vertebrates (Shu et al. 1999a). Their arthropod affinities are based on the segmented and jointed exoskeleton, and the transverse division of four skeletal plates: two lateral pleural plates and a dorsal and a ventral hard plate. The gill chambers are segmentally arranged in the pleural region, walled with membrane, and embedded within

Fig. 122 Pomatrum ventralis from the Early Cambrian Maotianshan Shale. (a) dorso-ventrally compacted abdomen showing a simple straight gut; (b) dorso-ventrally compacted, nearly complete specimen showing a short, conical mouth, segmented thorax, a jointed abdomen, and fine straight gut with terminal anus. Scale bar = 1 cm

the exoskeleton, resembling those of many living decapod crustaceans. The gill chambers are apparently modified exoskeleton, representing pharynxunrelated structures, in contrast to the pharynx-related gill pouches in the vertebrates. The exoskeleton of Vetulicola is not only thick, but is formed of a thin, dark outermost layer and a thick, pitted inner layer, comparable to the exoskeleton in the arthropod epicuticle (Brusca and Brusca 2002). However, the differences between the vetulicolids and the arthropods are also great. For instance, the vetulicolid head is short, simple (lacking eyes and other structures), and non-segmented, with a mouth situated at the terminal end. The thorax and appendages are fully enveloped by the exoskeleton (the gilled chambers are interpreted

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Fig. 123 Heteromorphus confuse from the Early Cambrian Maotianshan Shale. (a) restoration; (b) a nearly complete specimen, showing gilled chambers in thorax and segmented abdomen; (c) a nearly complete specimen showing gilled

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chamber in the thorax and a flattened abdomen; (d) a dorsoventrally compacted abdomen, showing a large terminal segment, hemicircular in outline. Scale bar = 1 cm

Fig. 124 Yuyuanozoon magnicissimi from the Early Cambrian Maotianshan Shale. Scale bar = 6 cm

as modified exopods). We here propose that the vetulicolids are an extinct panarthropod group with a close affinity to the arthropods. The loss of the endopods in the thorax and the development of modified exopods concealed within the exoskeleton suggest that the group may have adapted for pelagic life.

A Stalked Animal: Dinomischus and Its Possible Affinities Dinomischus is a Cambrian mystery, known from both Middle Cambrian Burgess Shale, Canada (Conway Morris 1977b), the Kali biota, Guizhou, China (Peng et al. 2006), and the Lower Cambrian

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Maotianshan Shale, Yunnan, China. Dinomischus in the Maotianshan Shale is represented by D. venustus (Chen et al. 1989b; Chen and Erdtmann 1991; Chen 2004). It is a solitary sessile organism, ranging from a few centimetres to 10 cm in height, and attaches to the sea floor by a stalk (Fig. 125). The stalked calyx-like body looks loosely like a flower and is enclosed by a whorl of 18 short petal-like plates. The petals are solid, plate-like structures (Fig. 126), smooth externally with elongated folds to provide strength (Fig. 127c). The inner surfaces of the petals are transversely wrinkled (Fig. 126), presumably representing the attachment sites for ciliary bands, playing a role in creating currents that facilitate food collection and its transport to the mouth. These petals are preserved in either an upright state (Fig. 126) or extended horizontally (Fig. 127), suggesting that they are jointed to the calyx at their proximal ends. These movable petal plates form a feeding bowl of adjustable size. In addition to its petal plates, D. venustus had an elongated, hard sclerite plate (Fig. 126), extending distally from the lateral margin of the calyx and

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presumably jointed to the lateral margin of the calyx at its proximal end. This plate probably acted as a backstop against the current, suggesting that the animal favoured environments in which the current was oriented in a single direction. The flower-shaped feeding bowl plays a role in down-current feeding. The mouth and anus occur next to one another within the feeding bowl. The flow bringing food enters the feeding bowl from the rear, passing through the spaces between the petal plates and flowing away with the waste water. The ciliary bands on the inner surface of the petal plates act in the food collecting by wafting food particles and prey downward to the mouth.

Affinities Dinomischus shows close affinity to the extant Kamptozoa (= Entoprocta), sharing a number of key characters, including a stalked calyx-like body, a downstream feeding mechanism, and a U-shaped gut with the mouth and anus positioned within the feeding bowl. Kamptozoa (= Entoprocta) is a small phylum, represented by 150 living species, all less than 1 mm in size, much smaller than Dinomischus. Most living kamptozoans are colonial in habit and their bodies are very soft.

Brachiopods

Fig. 125 Restoration of Dinomichius venustus (from Chen 2004)

The Brachiopoda constitute a phylum of solitary marine animals; they are also known as “lamp shells”. Although there are only 300 living species today, they have rich evolutionary history as they were the most diverse and prolific group of invertebrates in the Palaeozoic seas. The soft body is protected by a pair of mineralized dorsoventrally oriented valves referred to as the brachial or dorsal valve and the pedicle or ventral valve. The former houses the brachidium (lophophore) and gut while in the latter is the stalk or pedicle for attachment to the substrate. The pedicle valve has the opening from which the predicle itself protrudes. In the few forms without a pedicle, the pedicle (or ventral valve) is cemented directly to a hard substrate. The phylogenetic position of the Brachiopoda remains controversial. Although molecular studies have excluded the brachiopods from the deuterostomes, they do share a number of characters that are

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Fig. 126 Dinomichius venustus from the Early Cambrian Maotianshan Shale. Part (a) and counterpart (b) of holotype, and enlargement of petals, showing wrinkled inner surface (c). Scale bar = 1 cm

unique to the deuterostomes (Nielsen 2001). These characters include an apical organ containing several to many serotonergic cells, in contrast to the protostomes, which have only a few (2–3) serotonergic cells;

an apical organ either absent or not incorporated into the adult nervous system; the archimeric body typical of the deuterostomes, with a well-developed protocoel in the lava of Crania, a mesosome that sends canals to

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Fig. 127 Dinomichius venustus from the Early Cambrian Maotianshan Shale showing the feeding bowl in widely extended state. Scale bars = 0.2 cm (a, b) and 1 cm (c)

the tentacles, and a blastopore situated at the posterior end and closed in later larva, with the mouth opening at the opposite end in living Crania. Brachiopods in the Maotianshan Shale occur as two different forms: infaunal or endobenthic lingulaceans and epibenthic discinaceans. The shells in both forms are chitinophosphatic and have a pedicle. The endobenthic lingulaceans anchor to the bottom of their burrows by relatively long, elastic pedicles, whereas the pedicle in the epibenthic discinacean Heliomedusa is short, protruding through a slit in the pedicle valve and attaching to a hard substrate.

The lingulaceans in the Maotianshan Shale are represented by Lingulella chengjiangensis (Jin et al. 1993), Lingulellotreta malongensis (Rong 1974; Holmer et al. 1997; Zhang et al. 2004, 2006), and Longtancunella chengjiangensis (Hou et al. 1999). L. chengjiangensis (Fig. 128) is common in the Maotianshan Shale and its shell is small (8–12 mm long), elongated, triangular, and gently convex. The embo is rounded, about 1 mm in diameter. The pedicle valve has a narrow but relatively tall pseudointerarea, with a pedicle foramen at its peak. The pedicle is slender, fairly long. Internal muscles form a shield-shaped

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Fig. 128 Ligulella chengjiangensis from the Early Cambrian Maotianshan Shale showing the elongate shell with a slender, fairly long pedicle. Scale bar = 1 cm

Fig. 129 Lingulellotreta malongensis from the Early Cambrian Maotianshan Shale. Scale bar = 0.5 cm

muscular area, a heart-shaped umbonal scar, and a small, triangular, central muscle scar. L. malongensis (Fig. 129) has a small (7 mm) oval-shaped shell that is long and distinctly convex, adorned with discontinuous costae. The pseudointerarea in the pedicle valve is distinctly concave, with a pedicle groove in the apical part of the homeodelthyrium. The pseudointerarea is short, with a medial slit in the brachial valve. The interior of the brachial valve has a fan-shaped muscle scar divided into two parts by a narrow groove and enclosed by two lateral ridges posterolaterally. L. chengjiangensis has a large oval shell, 2 cm in diameter, adorned with fine, radially extended ribs, with a short, stout pedicle (Fig. 130). Heliomedusa orienta from the Lower Cambrian Maotianshan Shale (Figs. 131 and 132) is here regarded as a discinoid brachiopod and is the dominant form in the epibenthic community of the Maotianshan Shale fauna. It was first described as a medusa by Sun and Hou (1987) as is reflected in the genus name; in 1992 it was reinterpreted as a craniopsoid brachiopod by Jin and Wang (1992). Based on its many discinoid characters, it was redescribed as a discinoid brachiopod by Chen et al. (2007a). These characters include a longitudinally oval pedicle foramen; a short but stout

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Fig. 130 Longtancunella chengjiangensis from the Early Cambrian Maotianshan Shale. (a) showing compressed shell and stout pedicle; (b, c) showing radially extended ribs

pedicle descending ventrally from the pedicle valve; a paired rectus in the large pedicle canal; elongated scars of paired anterior adductor muscles; and a median septum connected to a U-shaped ridge on the ventral interior. The shell is thin and sub-circular in outline. The convex dorsal valve has a sub-marginal umbo with mixo-peripheral growth, and a unique pseudointerarea protruding from the posterior end. The ventral valve is flat, with a slight outward bulge in the anterior and lateral regions around the foramen, and a sub-central umbo with holo-peripheral growth anterior to the anterior rim of the elongate, oval-shaped pedicle foramen. The entire mantle borders of both valves are aligned with the setae. The lophophore occupies a large portion of the mantle cavity and comprises two brachia, in a simple design referred to as “trochophore”, with fewer than 20 hollow, ciliary tentacles in each brachium when young, become increasingly numerous in the adult (Zhang et al. 2003). The muscle scars comprise a pair of elongated anterior adductors and a pair of small posterior adductors. The pedicle is short, extending

ventrally from the foramen in the anterior region of the posterior sector of the ventral valve.

Non-chordate Deuterostomes The deuterostomes are morphologically well-defined groups of bilaterian animals. The criteria that define the non-chordate deuterostomes include the following: the blastopore becomes the anus in the adult; the apical organ has long cilia in its sensorial cells and contains many serotonergic cells that do not become integrated into the adult nervous system or contribute to the development of the adult nervous system; and the body is tripartite, including a prosome, mesosome, and metasome. The mesosome is a well-defined region, bearing tentacles. It is paired, surrounding the pharynx/oesophagus, and sends canals into the tentacles. In echinoderms, the left pouch is specialized as the hydrocoel, with radial canals extending into the podia. They probably represent a monophyletic group that

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Fig. 131 Heliomedusa orienta from the Early Cambrian Maotianshan Shale. (a, b) showing hollow tentacles and base of setae; (c, d) showing closely arranged tentacles. Scale bars = 0, 5 cm (a, c) and 1 cm (d)

arose from a common ancestor with bilateral symmetry, from which they evolved with diverse body plans as adaptations to different lifestyles. The non-chordate lower deuterostomes evolved in the Early Cambrian or even earlier, and diversified in the Early Cambrian. The Lower Cambrian Maotianshan Shale lies close to the root of deuterostome evolution, and preserves many distinct stemlineage deuterostomes. However, their relationships to modern phyla are difficult to ascertain and have been a controversial issue. In addition to brachiopods, two major groups of enigmatic Early Cambrian animals, a sessile (Phlogites) and a pelagic group (eldoniids), are possible deuterostomes. They have a crown of

hollow ciliated tentacles (also called a “lophophore”) encircling the mouth. The anus lies outside the tentacle crown but near it.

Sessile Lower Deuterostome Phlogites (=Cheungkongella) Phlogites Luo and Huo 1999 (=Cheungkongella Shu et al. 2001a) is a tentaculate bulb-shaped animal on a stalk (Fig. 133) with a spacious body cavity containing a coiled gut (Fig. 133a, b). The mouth opens within the feeding area and the anus at the end of the intestine is situated on the side of the calyx body (Fig. 133a, b); the latter is referred to as a “cloacal siphon”, although

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Fig. 132 Heliomedusa orienta from the Early Cambrian Maotianshan Shale. (a) enlargement of ventral valve showing pedicle foramen; (b) dorsal valve showing pedicle attachment

scar; (c) dorsal valve showing tentacle and pedicle attachment muscle scar; (d) dorsal valve showing anterior adductor muscle scar and ridge. Scale bar = 0.2 cm

Fig. 133 Phlogites longus from the Early Cambrian Maotianshan Shale. (a, b) counterparts of a nearly complete specimen showing branched tentacles, coiled gut within the coelomic cavitiy, anus on side of the body and a holdfast attached

to a trilobite genal spine; (c, d) showing branched tentacle (c) and large coelomic cavity (c, d). Scale bars = 1 cm (a–c) and 0.5 cm (d)

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it is not funnel shaped as that of the tunicate siphon. The hollow tentacles are branched; only incomplete parts of the tentacles are exposed at the surface of most specimens, making the total number remains unclear. Some specimens suggest three arms and others suggest five. Cheungkongella (Shu et al. 2001a) is a junior synonym of Phlogites (Luo and Hu, in Luo et al. 1999). It is based on a single incomplete specimen that is indistinguishable from Phlogites, although the authors claimed the presence of a pharynx. The irregularly arranged dotted pits on the darkly stained film are claimed to be gill openings, but appear to be artefacts of rock splitting. The “pharynx” is interpreted herein as a coelom. The “buccal tentacles” referred to by Shu et al. (2001a) are more likely to be a mouth because it opens at the body surface, rather than projecting above it. The Cheungkongella specimen does not show any obvious arms, perhaps because its arms have broken off or are covered by rock.

Phylogenetic Affinity Phlogites is interpreted as a lower deuterostome, sharing an archimeric body plan. Its mesocoel is externally recognizable by its large, branched, hollow tentacles; the metacoel is a spacious body cavity with an encased coiled gut.

Fig. 134 Restoration of Early Cambrian medusiform organism Stellostomites eurorphus

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Discoidal Pelagic Deuterostomes: Eldoniidae The eldoniids represent an extinct, monophyletic nonchordate deuterostome group, dominant among the Cambrian pelagic community, although some authors have considered them benthic (Dzik et al. 1997). They share a common body plan, characterized by a low bell-shaped body, with a convex upper surface and a concave lower surface. The upper surface is soft, supported by fine dorsal radii in Eldonia (which possibly lacks dorsal radii) and Stellostomites (Figs. 134, 135, and 136) or a possibly mineralized hard skeleton in Rotadiscus (Figs. 137, 138, 139, and 140) and Pararotadiscus (Zhao and Zhu 1994; Zhu et al. 2002). However, their internal anatomy is asymmetric and complex, with a sub-horizontally clockwise-coiled sac (when viewed from above). The alimentary canal is situated dorsally in the coiled sac, ending with a mouth and anus ventrally, both off centre on one side of the disc and close to each other. A crown of hollow, branched tentacles encircles the mouth. A hydraulic sac lies ventrally in the alimentary canal and is divided into numerous segmental parts. These hydraulic compartments extend radially, and each sac has a canal connected to the central ring canal and is bifurcated in its peripheral part. The lower surface is soft, with radial rows of elongated structures that correspond to the distribution of the radial canals (Fig. 140). These structures are 0.2 mm wide and 0.35 mm long, but

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Fig. 135 Stellostomites eurorphus from the Early Cambrian Maotianshan Shale showing: imbricate preservation (a), clockwise coiled sac with alimentary canal lying dorsally in the sac (a

“right one”, b, c), tentacles (c), central ring (b, c), radial canals (c), and triangular sac (c). Scale bars = 2 cm (a) and 1 cm (b, c)

the innermost one is much larger. They are comparable to the tube feet in echinoderms. The eldoniids represent an extinct basal deuterostome group with a complex water-vascular system. The system consists of tube feet, a radiating arrangement of internal canals and sacs, and a circum-oral ring canal at the centre of the discoidal body. Radial canals, bifurcating midway, extend to the peripheral margin of the discoidal body. Each of the radially extended vascular sacs has a bifurcated canal; its ventral surface has organic structures that are tubular outgrowths of the body wall, comparable to the tube feet of living echinoderms. These structures are arranged in a radial row, with a bifurcated shape on the surface ventral to the radial canal.

The bodies of the eldoniids are radially symmetrical externally, coiled, and sac like, encasing a complete gut. The gut is highly differentiated into a mouth, oesophagus, stomach, intestine, and terminal anus. The mouth is surrounded by a pair of branched, hollow, and possibly ciliated tentacles, forming a horse-shoelike feeding bowl with the opening facing forward. The animal is an up-current feeder. The current enters the feeding bowl from the open side, carrying food items, but leaves through the open spaces between the tentacles on the closed side of the tentacle crown. Eldoniids are recorded in both the Middle Cambrian Burgess Shale in Canada (Eldonia ludwigi) and recently in the Lower Cambrian Maotianshan

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Fig. 136 Stellostomites eurorphus from Early Cambrian Maotianshan Shale, showing branched tentacles (a) and radiant sacs (b). Scale bar = 2 cm

Fig. 137 Restoration of Rotadiscus grandis

Shale in Yunnan in southern China (Stellostomites eurorphus, Rotadiscus grandis; Chen et al. 1995d, 1996; Chen 2004) and the Middle Cambrian strata at Guoizhou (Pararotadiscus guizhouensis; Zhu et al. 2002). S. eurorphus (=Yunnanomedusa eleganta) (Figs. 134, 135, and 136) is the predominant element in the pelagic community of Chengjiang, but it is much less

common in Anning and is absent in Haikou. The animal has a low bell shape, weakly sclerotized, with a convex upper surface and a concave lower surface. A major part of the body is a sub-horizontally clockwisecoiled (top view) sac (Figs. 134 and 135), which encases a gut that extends parallel to and along the top surface of the sac and opens externally at both ends onto the lower surface of the discoidal body. The gut

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Fig. 138 Rotadiscus grandis from the Early Cambrian Maotianshan Shale showing: horseshoe-shaped tentacle crown and branched hollow tentacles (a, b), radial canals (a) and tube feet (a). Scale bar = 2 cm

is differentiated into the mouth, oesophagus, expanded stomach, and intestine. The mouth is surrounded by a pair of branched tentacles (Figs. 135c and 136a); these are hollow, possibly ciliated, and form a U-shaped feeding structure with a wide anterior opening, suggesting that the animal was an up-current feeder. The current not only brings food particles to the open side but also pushes the tentacles from the open side, creating an anticlockwise circulation in the discoidal body.

The spacious coiled sac is a well-defined structure located about midway between the centre and the margins of the disc and encasing the alimentary canal. The enclosed alimentary canal lies dorsally within the sac and is differentiated into the oesophagus, stomach, and intestine (Fig. 135b, c). It is spiral, generally in the same horizontal plane except for its anterior mouth and posterior anus, which open ventrally. The mouth is surrounded by a horse-shoe-shaped tentacle crown (Figs. 134, 135c, and 136a).

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Fig. 139 Dorsal view of a nearly complete Rotadiscus grandis from the Early Cambrian Maotianshan Shale showing growth lines and radially extended fine ribs. Scale bar = 2 cm

Fig. 140 Rotadiscus grandis from the Early Cambrian Maotianshan Shale showing tube feet and radial canals. Scale bars = 2 cm (a) and 0.5 cm (b)

The proposed anus opens at a point about midway between the centre and outer margin, with the anterior oral end located more centrally. The up-current feeding activity, with anticlockwise circulation, could effectively avoid the mixing of waste-laden water from the anus with food-laden water within the feeding bowl. The oesophagus narrows rapidly anteriorly and ends with a terminal constriction. The stomach is the most prominent part of the alimentary canal; it is strongly curved, occupying the broadest part of the alimentary canal diminishing in width both posteriorly and anteriorly. A conspicuous feature of the structure is its black stain, usually absent from the adjacent parts of the

intestine and from the underlying sac. The posterior end shows an abrupt contraction and the black stain usually terminates at this point. The posterior part of the digestive tract is elongated and is roughly as long as the stomach, with width equal to about one-half the maximum diameter of the stomach. The lower compartment of the sac, referred to here as the “coiled sac proper”, seems to be a vascular organ enclosed ventrally by radial sacs. The coiled sac is preserved as a yellowish structure, with no indication of black stain. The alimentary canal and the coiled sac proper appear to be of similar sizes. They overlap completely for their entire lengths as the result of vertical

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compaction, so only one of them is exposed at the surface (Fig. 135a). However, in a number of cases, a split reveals both structures. When compaction is in an oblique direction, the two structures only partially overlap, producing an elongated zone of overlap within the outline of the sac (Fig. 135a on the right, and b, c). The borders are well defined and probably represent the mesenteria of the alimentary canal. The water-vascular system is highly developed, consisting of a central ring and radially extended sacs and canals. Each of the radially extended vascular sacs has a bifurcated canal and rarely preserved black dotted structures representing tubular outgrowths of the body wall, comparable to the tube feet of living echinoderms. The sclerites are apparently external structures, attached to the outer surface of the ventral cuticle. These structures are arranged in radial rows, with a bifurcated shape on the surface ventral to the radial canal. They are usually detached after the death of the animal. In most cases, they are either entirely absent or only partly preserved. They appear to have a sub-circular base and are elongated distally, 0.2 mm wide and 0.35 mm long, except for the innermost one, which is considerably larger. The animal has two sets of radially extended structures, a dorsal and a ventral set, which function in support and as water-vascular structures, respectively. There are 44 ventral radii radiating from the central ring canal to the periphery on the same plane throughout the ventral part of the coiled sac. Their course, which is otherwise strictly radial, tends to diverge from radial in the area adjacent to the ventral depression. A pair of auxiliary canals is added to each of the primary canals at its mid length, approximately at the outer margin of the coiled sac. The ventral radial canals are encased by radially extended sacs. Each of the sacs encases a branched ventral canal. In most cases, the dorsal surface is supported from below by the ventral canals and tends to maintain a positive relief, whereas the original shape of their ventral surfaces is completely obliterated. The central part of the discoidal body has a cavity that is enclosed by a rigid, ridged membrane dorsally and by a soft membrane ventrally. The ventral membrane tends to be lower ventrally, forming a triangular depression (Fig. 135c). The central cavity is probably a component of the water-vascular system.

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The tentacle crown consists of two arm-like ridges, tentacle-carrying organs that curve into a horse-shoelike form in outline. The two tentacles growing out from the organs are branched dichotomously many times, forming fairly fine branches distally. The wall of the convex, inferred dorsal surface of the animal is distinctly defined, displaying fine concentric lines in some specimens. These concentric lines are interpreted as growth lines and are evenly spaced, at about 0.1 mm, throughout the entire dorsal surface. Identical growth lines are also observed in Rotadiscus. The wall of the concave ventral surface of the body is thinner but also bears fine concentric lines, interpreted as growth lines, densely spaced at the same distance as seen on the dorsal epidermis. An annular band, interpreted here as possible concentric muscle markers, is formed by a group of concentric raised riblets, about 2–4 mm wide, located at one-fifth of the disc radius from its outer margin. It lies ventral to the dorsal set of radial canals but dorsal to the radial sacs. The riblets of the annular band appear to be rigid and rough. The dorsal epidermis is soft and supported by a set of 88 fine radii, which are stiff and extend radially to the periphery of the discoidal body. They are about 0.1–0.2 mm in diameter. R. grandis (Sun and Hou 1987) is a large discoidal eldoniid (15 cm in diameter), having a hard, possibly mineralized dorsal cover (Fig. 137). The dorsal cover has both fine, radially extending lines and concentric growth lines (Fig. 139). The animal has only one set of radii, corresponding to the ventral radii in S. eurorphus. There are 88 radial canals, extending from the central canals and ending in a pair of auxilliary canals midway along the radius (Fig. 138a). Ventral to the radii are hollow, linearly arranged tube feet, 0.5 mm in diameter (Fig. 140). Like S. eurorphus, the major body region of R. grandis is a horizontally extended, clockwise-coiled sac, encasing the alimentary canal, which is differentiated into a mouth, an oesophagus, a stomach, an intestine, and an anus. The mouth is surrounded by a horse-shoe-shaped tentacle crown composed of two tentacle-bearing organs, each with 13 tentacles (Fig. 138b).

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Affinities The phylogenetic affinity of the eldoniids, especially Eldonia, has evoked much controversy since 1911, when it was originally described as a holothurian (Walcott 1911a) or considered an echinoderm (Clark 1912; Croneis and McCormack 1932). The interpretation of Eldonia as a holothurian, introduced by Walcott (1911a), remained popular for a long time (Durham 1974). Duncan Friend evoked it again, pointing to its similarities to a group of extant deep-sea pelagic holothurians (see Gee 1992), although the echinoderm affinity of Eldonia has been queried by other authors (Paul and Smith 1984; Chen et al. 1995d; Dzik 1989). The marginally accreted external skeleton and no sign of either pentamerous symmetry or an endoskeleton in the eldoniids suggest that they cannot be attributed to the Echinodermata, but rather to the pre-echinoderm deuterostomes (Conway Morris 1998). The eldoniids have a well-developed water-vascular system, including a central ring canal, radial sacs and canals, and tube feet. A clockwise-coiled sac encases the digestive tract. The group is not consistent with any recognized deuterostome. The eldoniids show affinity to Phlogites in having a large main body cavity, housing a coiled gut, but they differ from Phlogites in having a highly developed water-vascular system, including a central ring canal, radial sacs and canals, and tube feet. They show close affinities to the echinoderms with which they share several key characters, such as external radial symmetry, a coiled alimentary canal, and a highly developed water-vascular system that includes a central ring canal, radial canals, and tube feet. However, the differences between them are great. For instance, eldoniids are perfectly radially symmetrical; they lack an endoskeleton; and they have marginal excrementary growth, suggesting that the eldoniids represent a pre-echinoderm stage in deuterostome evolution (Conway Morris 1998). The eldoniids also share characters with the brachiopods, such as the marginal excrementary growth of the exoskeleton, but their differences from them are great. For instance, the body of the brachiopod is well protected both dorsally and ventrally by mineralized valves, and its main body cavity (metacoel) sends extensions into the mantle folds and stalk, and the water-vascular system is not developed. For these reasons, we reinterpret the eldoniids as a stem-lineage

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deuterostome group that evolved with the echinoderms from a common ancestor, but adapted to a pelagic lifestyle rather than to a sessile lifestyle.

Non-vertebrate Chordates: Shankouclava Tunicates (sea squirts) and their planktonic relatives form a subphylum (Urochordata) of the Chordata, but they resemble other chordates only very slightly. They are usually sessile (e.g. Fig. 141a), and with the exception of the planktonic form (Appendicularia), their chordate characters, including the notochord, hollow dorsal nerve cord, and post-anal tail, only occur in the transitory larva, called the “tadpole”. The subphylum Urochordata was previously interpreted as the most basal branch of the known

Fig. 141 Extant urochordate (a) and restoration of Early Cambrian urochordate Shankouclava anningense. (a, courtesy of D. Weber)

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chordates. However, recent molecular data have shown that this subphylum is a sister group to the Vertebrata (Delsuc et al. 2006; Schubert et al. 2006) and that both evolved from an amphioxus-like ancestor but adapted to different lifestyles, a sessile inactive lifestyle in the tunicates and a more active lifestyle in the vertebrates. The discovery of both fossil vertebrates and tunicates in the Lower Cambrian Maotianshan Shale implies that chordates had already differentiated into three major groups during the Early Cambrian or even earlier, comparable to the extant cephalochordates, tunicates, and vertebrates probably explaining why the tunicates have diverged morphologically furthest from the chordate ground plan. The fossil record of the tunicates is also fairly limited. The Lower Cambrian tunicate Shankouclava anningense (Chen et al. 2003b) is the only known reliable fossil representative of the tunicates. The Lower Cambrian Phlogites (= Cheungkongella) is said to be a tunicate (Shu et al. 2001a), but it differs from the tunicates in lacking a pharynx and by the presence of long branched tentacles (a distinctly non-tunicate feature) (Shu et al. 2001a), and probably represents a basal branch of the lower deuterostomes (Caron et al. 2010). Another so-called tunicate fossil, Jaekelocarpus, from the Carboniferous is covered with large calcite plates instead of a tunic, and its supposed branchial bars have an unusual coronal orientation, so a tunicate identity is unlikely. Shankouclava shankouense from the Lower Cambrian Maotianshan Shale (Shankou, Anning, near Kunming) is a solitary sessile tunicate. It is a soft-bodied, club-shaped animal, elongated (2–4 cm long), and pointed proximally, with attachment stolons indicating it was sessile and rooted to the ocean floor by these structures (Fig. 141b). The body is bipartite, with a barrel-shaped anterior part and a triangularly elongated posterior part, called the “abdomen”. The anterior part, which occupies more than half the length of the body, is dominated by a large pharynx, with up to 30 branchial bars (Fig. 142). The branchial bars branch to form a rectangular network with stigmata (branchial openings). An oral siphon opens subventrally, containing oral tentacles at its base. An endostyle band extends along the mid-ventral part of the pharynx, and a sac-like atrium surrounds the pharyngeal basket (Fig. 143a). The alimentary canal is U-shaped, with the anterior gut (oesophagus) running

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posteriorly from the pharynx and forming a loop, called the “stomach”, near the base of the abdomen. From there, the posterior gut (intestine) extends anteriorly, ending near an atrial pore lying two-thirds of the way back from the anterior pharyngeal margin. This Cambrian animal resembles the tunicates to some extent, in its tunic and mantle, the large perforated pharyngeal region with numerous transversely oriented structures, branchial bars, the sac-like peripharyngeal atrium, the oral siphon with what appear to be oral tentacles at its base, the dorsal atrial pore, and the elongated endostyle band on the midventral part of the pharynx. Its resemblance to the single zooids of modern colonial aplousobranch tunicates, such as Clavelina and Amaroucium, is striking. Like Shankouclava, the bodies of Clavelina and Amaroucium are slender and differentiated longitudinally into two parts of sub-equal length, with a notched constriction between them. Shankouclava differs from the aplousobranchs in that its atrial pore opens further posteriorly on the pharyngeal roof. However, the discovery of the Lower Cambrian Shankouclava (Chen et al. 2003b) indicates that the tunicates had already diverged morphologically from the main evolutionary course of the vertebrates by the Early Cambrian. Despite its departure from the main vertebrate evolutionary line for more than half a billion years, and the lack of any crucial features in either its body plan (Lacalli 2005) or genome (Holland 2007) that link it directly to the vertebrates, the tunicates still offer many interesting clues to the evolutionary origin of the vertebrates, with respect to the neural crest cells (Jeffery et al. 2007), brain (Dufour et al. 2006), heart (Simões-Costa et al. 2005; Davidson and Levine 2003), and eye lens (Shimeld et al. 2005).

The First Vertebrate Fossils Fill a Gap in the History of Evolution of the Vertebrates The Cristozoa (also known as “crest animals”) represents those animals containing a neural crest and its derivatives and includes all known craniates and their immediate pre-craniate ancestors. The pre-craniate crest animals are all extinct and are preserved only in the Early Cambrian strata of Yunnan (south-western China). The fine anatomical details of Haikouella

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Fig. 142 Holotype of Shankouclava anningense from Early Cambrian Maotianshan Shale. (a) and (b) are counterparts. Scale bar = 0.5 cm

and the slightly more advanced species Yunnanozoon show many characters unique to the vertebrates, but lack a skull and most other elaborated placodal and neural-crest derivations, throwing new light onto the previously missing history at the very beginning of cristozoan evolution. A comparative study of the cephalochordate amphioxus suggests that pre-craniate evolution was marked by a series of innovations, including muscular ventilation with gill-bearing and

jointed branchial arches; paired head sensorial organs, including paired eyes and nostrils; a relatively large, slightly differentiated brain; protovertebrae; and some derivatives of the neural crest cells. However, the pre-craniate crested animals lack ears, a clear telencephalon, and a skull. Furthermore, a comparison of the brains of amphioxus and the craniates suggests that the tripartite brain with a telencephalon is not the older structure, but a novelty of the craniates.

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Fig. 143 Shankouclava anningense from the Early Cambrian Maotianshan Shale. (a) laterally compacted specimen showing endostyle and coiled gut with anal opening on opposite side to

endostyle; (b) side view of a partially preserved specimen showing tunic, mantle, and branchial bars (both left and right sets). Scale bar = 0.2 cm

The vertebrae and skull are widely accepted as the two major features defining the vertebrates. However, these two criteria did not evolve synchronously. The skull was previously considered an evolutionarily older structure than the vertebrae (Janvier 1978). In contrast, the Lower Cambrian fossils Haikouella lanceolata, Yunnanozoon lividum, and Haikouichthys ercaicunensis all have protovertebrae but no clear skull, suggesting that the vertebrae are evolutionarily deeply

rooted, representing a structure older than the skull. The lack of vertebrae in the living hagfishes is probably a derived feature. To avoid the ambiguity entailed when either the vertebrae or skull are used as characters defining the vertebrates, Holland and Chen (2001) proposed the term “Cristozoa”, or crest animals, to represent those animals with a neural crest and its derivatives. These Cambrian animals had jointed cartilagenous

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branchial arches, pharyngeal teeth, and evidence of muscular ventilation, implying that they had definitive neural crest cells and were crest animals (Holland and Chen 2001; Mallatt and Chen 2003; Holland and Holland 2001). The Cristozoa includes the craniates and their immediate ancestors, the pre-craniate Cristozoa. Among the Early Cambrian crest animals, Haikouella is one of the most remarkable. Its soft tissues and organs are not only preserved in extraordinary detail, but it also represents a crucial evolutionary position close to the nexus between an amphioxus-like ancestor and the vertebrates, at the very beginning of the Cristozoa (Chen 2008, 2009). These early preserved cristozoans have numerous vertebrate characters: paired eyes, nostrils (preserved only in Haikouella), a distinct head with upper and lower lips (only seen in Haikouella), jointed branchial arches with paired gill rays, pharyngeal denticles, and protovertebrae, supporting a close affinity with the vertebrates. However, unlike vertebrates, these animals lack a skull, ears, a clear telencephalon, and most other elaborated placodal and neural-crest derivations. They are also similar to the living cephalochordate, amphioxus, in both their general external aspects and in some specific characters, including their oral tentacles, endostyle, and large notochord. All these factors strongly suggest that Haikouella and Yunnanozoon represent a missing evolutionary link at the dawn of the vertebrates, before the rise of the craniate vertebrates.

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Cristozoans were diverse in the Early Cambrian, and included H. lanceolata, Y. lividum, and H. ercaicunensis, each representing a different evolutionary stage in the evolution of the craniate vertebrates. Among them, H. lanceolata is the most primitive and its occurrence is restricted to Haikou (Fig. 144), Kunming, where it is fabulously preserved in great anatomical detail. It also represents a basal position in the evolution of the crest animals. The anatomy of these early cristozoans is crucial to our new understanding of the ground plans of the vertebrates and of their brains, heads, head sensorial organs, branchial arches, backbones, and feeding behaviour (Fig. 144). H. lanceolata is 2.5–3 cm long (maximally 4 cm) and lanceolate in outline, flattened ventrally in its anterior portion but compressed laterally in its posterior portion. The pharyngeal system has only six postmandibular arches and the three mandibular arches are missing. Instead of mandibular arches, Haikouella has mandibular aortae. It has only four pairs of gonads. The pharyngeal teeth are situated ventrally in the mid pharyngeal cavity. The myotome consists of 25 myomeres, separated by simple straight myosepta. Y. lividum (Fig. 145) is restricted to the Chengjiang area. It was previously thought by Hou et al. (1991) to be problematic, with unknown affinities, and was interpreted as a possible chordate by Chen et al. (1995a). However, Chen recently reinterpreted Yunnanozoon as an early crest animal, with close

Fig. 144 Restoration (a) and illustration of anatomical characters (b) in Haikouella lanceolata

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Fig. 145 Yunnanozoon lividum from the Early Cambrian Maotianshan Shale. (a) restoration; (b, c) counterparts of a nearly complete specimen. Scale bar = 0.5 cm

affinity to H. lanceolata. The animal has paired mandibular branchial arches (Fig. 145), larger lateral eyes (Fig. 150) than H. lanceolata, and much larger pharyngeal denticles (Fig. 153C–D), suggesting that Yunnanozoon is evolutionarily more advanced than H. lanceolata (Chen 2004, 2008, 2009). The animal is 3–4 cm long, lanceolate in form, and compressed laterally. The pharyngeal system consists of seven pairs of segmented branchial arches, thicker than those of H. lanceolata, separated by wide branchial slits. Each segment of the branchial arches bears a pair of gill rays. Simple, cone-shaped denticles, about 1 mm long, occur on the pharyngeal floor at the base of the pharynx in Yunnanozoon. The myotomes are divided by simple straight myosepta into 23 repeated segmental structures, known as muscle segments (“myomeres”). The 13 pairs of gonads occur on the lateral surface of the foregut (Fig. 145b, c). H. ercaicunensis (Shu et al. 1999b; Fig. 146) cooccurs with Haikouella, restricted to the Haikou area. It is lanceolate and only 2.5 cm long. The head is small,

with a pair of lateral eyes, a possible nasal capsule, and an auditory capsule. The pharynx consists of 6–7 pairs of branchial arches. The myosepta are W-shaped. H. ercaicunensis has a prominent dorsal fin with fin radials, similar but not the same as those of the hagfish and lamprey. The 13 circular structures along the base may be gonads. The animal is interpreted as a primitive craniate, but it has no clear skull and its craniate identity is questionable. However, the animal has Wshaped myosepta, large lateral eyes, and a prominent dorsal fin with fin radials (Fig. 146b), suggesting that it is the most advanced form of the Lower Cambrian crest animals, representing a turning point in the transition from procraniates to craniates. Although some researchers have considered Yunnanozoon and Haikouella hemichordates or lower deuterostomes, or problematic organisms with unknown affinities (Shu et al. 1996, 2003b; Conway Morris 2000; Smith et al. 2001), their conflicting views have been clarified by a number of studies (Mallatt and Chen 2003; Chen 2008, 2009).

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Fig. 146 Haikouichtys ercaicunensis from the Early Cambrian Maotianshan Shale. (a), restoration; (b) holotype. Scale bar = 0.5 cm

Haikouella Sheds Light on the Ground-Plan of the Head of Crested Animals The head accommodates the sensorial and feeding organs externally and the brain internally. It is fundamental to the evolutionary changes from the amphioxus-like ancestor to the craniate. The head in the ancestral condition, as exemplified by the living amphioxus, is simple and characterized by a short, blunt, anterior projection, known as the “rostrum” (Fig. 147), with which the animal pushes aside the sand while burrowing (Fig. 148). The pre-mandibular oral cavity has a ventrally located mouth, surrounded by tentacles. The mouth is protected dorsally by the rostrum but there is no lower lip (Fig. 147c). None of the elaborated paired sensorial organs of the craniates existed in the amphioxus-like ancestor. In contrast to the simple ancestral head, the craniate head is a complex and unique structure, including a cartilagenous or bony skull that encases the brain, paired sensory organs, and an oral cavity, with a premandibular mouth surrounded with upper and lower lips. The great contrast between the simple amphioxus-like head and

the complex craniate head implies the existence of unknown intermediate forms. The head in the early crest animals, as exemplified by Haikouella (Fig. 149) and Yunnanozoon, probably fills the gap between the simple amphioxus-like head and the complex craniate head. It has paired eyes, possible olfactory organs, a large brain, and a mouth surrounded by upper and lower lips (Fig. 149), and is thus much more complex than the head of amphioxus (Fig. 147c). However, the head in the early crest animals lacked a clear skull and ears, so it was simpler than that of the craniates. The mouth is surrounded by both an upper dorsal lip and a lower ventral lip in the early crest animals (Haikouella): these might have functioned to prevent the escape of the semi-sessile soft-bodied prey upon which the animals presumably fed. The lower lip is a novelty in the vertebrates, but the upper lip is deeply rooted in an amphioxus-like ancestor. The anteriorly extended rostrum in amphioxus might be the precursor of the upper lip. It is a robust structure, strengthened by the anteriorly extended notochord (Fig. 147c), and presumably has multiple functions, including in the protection of the mouth during burrowing with its

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Fig. 147 Extant cephalochordate Branchiostoma belcheri Gray from the South China Sea. (a, b) side views (left and right) of an individual; (c) view from the left side of anterior portion of the body. Scale bars = 2 mm (a, b) and 200 μm (c) Fig. 148 Lifestyle of the extant cephalochordate Branchiostoma belcheri. (a) swimming; (b, c) burrowing in sand with head exposed; with tail (c, d) and head (e) first, respectively, while burrowing. (d, c) with the tail (d) and head (e), respectively, first while burrowing

pointed end (Fig. 148e) and possibly in the collection of olfactory information. The oral cavity in the early Cristozoa, as exemplified by Haikouella, is situated in a premandibular position, with a circular mouth opening surrounded

by an oral skeletal ring and tentacles, exactly as in amphioxus (Fig. 147c). The premandibular oral cavity and mouth (known as the “old mouth”) represent the primitive condition in the chordates. The “old mouth” occurs not only in the cephalochordates and tunicates

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Fig. 149 Head and its sensorial organs in Haikouella lanceolata from the Early Cambrian Maotianshan Shale showing paired eyes (a, c, d), paired nostrils (a–d), diencephalon and hindbrain (a, b), mouth (a–d), tentacles (c, d), upper and lower lips (b– d), oral cavity (c, d), and gill rays internal to the branchial

arches (b). Abbreviations: Dn, diencephalon; Hb, hindbrain; Mo, mouth; Nt, nostrils; Sn, snout; Mhp, first (mandibulo-hyoid) gill pouch; Ul, upper lip; Ll, lower lip; F(h)b, first (hyoid) branchial arches; Ma, mandibular aorta Note: d is counterpart of c. Scale bar = 1 mm (adapted from Chen 2008)

but has also continued into more advanced forms, including the pre-craniate crest animals, agnathans, and some lower gnathans (Mallatt 1996). The oral cavity in Haikouella has an external mouth opening at in front, with a diameter of about 1 mm, identical to that in amphioxus. The mouth is surrounded by a skeletal ring that supports the oral tentacles (Fig. 149c, d). The oral-labial region in Haikouella has distinct upper and lower lips, probably representing a novelty in the crest animals. The oral-labial region in the cephalochordate amphioxus lacks a homologue of the vertebrate lower lip but has a large rostrum projecting dorsoanteriorly. The rostrum in amphioxus is not strengthened by a muscular structure, as seen in the crest animals, but is supported by the

notochord, extending anteriorly to the pointed end of the rostrum (Fig. 147c). The rostrum is probably used by amphioxus to burrow with its pointed end and is presumably the precursor of the upper lip in the early Cristozoa. The upper lips in Haikouella are large and paired, probably representing muscular structures (Fig. 149c, d). An identical structure also appears in the lamprey larva, hagfishes, and some soft-boned fishes. Unlike the rostrum with its pointed end in amphioxus, the upper lips in Haikouella are broadly rounded and do not function for burrowing, but are probably used to probe for prey with the help of its olfactory senses. These prey might include algae, embryos, larvae, and small animals living near the surface or shallowly within the sediment. The lower lip in Haikouella is a

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conspicuous structure and has none of the homologous structures seen in the protochordates, but appears in the lower craniates, including the jawless fishes (larval lamprey and hagfishes) and some soft-boned fishes (chimaeroids and some sharks; Mallatt 1996). It is a novelty in the crest animals (Mallatt and Chen 2003). Oral tentacles occur in the cephalochordate amphioxus and some living ascidians (Brusca and Brusca 2002) and also in the Early Cambrian tunicate S. anningense (Chen et al. 2003b). They are used to prevent larger food and sand particles from entering the mouth. The tentacles in amphioxus are numerous (up to 40), very fine (40 μm in diameter), and narrowly spaced (about 40 μm; Fig. 147c), suggesting that amphioxus feeds on food grains smaller than 40 μm, mainly single-cell algae. Oral tentacles also occur in Haikouella, presumably resembling those in amphioxus and forming a screen to prevent larger food and sand particles entering the mouth. However, they are relatively more robust (250 μm in diameter) and fewer in number (about 12 in total), with relatively wider spacing, with about 300 μm between two adjacent tentacles (Fig. 149c, d). The tendencies of the oral tentacles to become increasingly robust, to become more widely spaced, and to decrease in number presumably correspond to a shift to increasingly larger food grains during the transition from an amphioxus-like pre-cristozoan ancestor to the cristozoan animals. The wider spacing in Haikouella indicates that the animals could ingest coarser food grains, up to 300 μm in size, including sea weeds, embryos, larvae, and microscopic animals.

Head Sensory Organs The ground plan for the head sensory organs in the crest animals has been a controversial issue. The rise of uniquely vertebrate sensory organs has been postulated in a serial transformation model by Butler (2000, 2006) and other authors (Northcutt and Gans 1983; Gans 1993), in opposition to the notion that all the craniate sensory organs elaborated simultaneously when the pre-craniates became predators. Amphioxus lacks a vertebrate-type head sensory organs but has a simple non-image-forming front eye (Fig. 147c), possibly the precursor of paired eyes. It also lacks an identifiable olfactory organ and has no hearing organ, but some molecular data suggest

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that the rostrum in amphioxus has an olfactory sense (Glardon et al. 1998). Haikouella has both paired eyes (Fig. 149a–c) and possible paired nostrils (Fig. 149a), and it conforms well to Butler’s model, predicting that the eyes are older structures and all the craniate sensory organs were not elaborated simultaneously (Butler 2000, 2006). The eyes in the early crest animals, as exemplified by Haikouella, Yunnanozoon, and Haikouichthys, are regularly rounded and relatively large, at about 0.2–0.4 mm in Haikouella (Mallatt and Chen 2003; Chen 2004), 0.6 mm in Yunnanozoon (Chen 2004), and 0.4 mm in Haikouichthys (Shu et al. 1999b, 2003a). The visual organs in amphioxus are represented by the front eye (Fig. 147c), located at the rostral end of the nerve cord and consisting of a pigment cup, two rows of uniciliate sensory cells (presumably photoreceptors) behind it, and two rows of neurons further behind them (resembling retinal amacrine and bipolar cells, respectively) (Lacalli et al. 1994; Lacalli 1996; Wicht and Lacalli 2005). The front eye is presumably the homologue of the vertebrate paired eyes based on the general similarity of their cellular organization and the similarity of the front eye to the developing vertebrate eye, represented by a single medial primordium. The front eye is very small and simple (only 10 μm in diameter in the larva and about 20 μm in the adult), with its neurons arranged transversely in single rows. As the eye has only a one-dimensional receptor field, it is not an image-forming organ (Lacalli et al. 1994). In contrast to amphioxus, the large eyes in these Early Cambrian cristozoans might resemble those of extant vertebrates, as they have many more neurons packed in layers, probably forming two-dimensional receptor fields allowing proper image development (Lacalli et al. 1994). The origin of the eyes, especially the complex, image-forming eyes, has received special attention. The tool-kit of genes that participate in building the eyes are shared among the bilateral animals, placing the origin of the eyes in the common ancestor of the bilateral animals. In contrast to this prediction, imageforming paired eyes are not present in most animal groups, but arose independently among only a few, distantly related animal groups, including the molluscs, arthropods, chordates, and annelids. The sudden emergence of image-forming eyes among these distantly related animal groups is intriguing and it has recently been interpreted as a response to increased

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predation and visual hunting (Fortey et al. 1997; Parker 1998). However, the first arthropods, as exemplified by the Lower Cambrian Fuxianhuia and Shankouia, were definitely not active predators but inactive suspension and microphagous feeders, although these animals had large, paired, image-forming eyes. The paired eyes are a novelty of the crest animals and the first crest animals, exemplified by Haikouella and Yunnanozoon, were definitely not active predators. The development of elaborated, image-forming eyes in both the arthropods and crest animals in Cambrian times was probably triggered by an intensified “arms race” in predators and prey, with the emergence of visual hunting in the predators and of visual feeding and escape in the prey.

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in the vertebrate olfactory bulb occur in the anterior nerve cord of amphioxus (Moret et al. 2004). The rostral pathway in amphioxus may be homologous to the olfactory nerve (Lacalli 2004). The preservation of possible paired nostrils (Fig. 149a–d) and related olfactory bulbs (Figs. 150 and 151b–c) in Haikouella argues for the origination of an elaborate olfactory system, including paired nostrils and paired enlarged olfactory bulbs, which appeared simultaneously with elaborate paired eyes in the early evolutionary stages of Cristozoa. The primitive nostrils, exemplified in Haikouella, are paired (Fig. 149a), with a dorsal and anterior location at the anterior margin of the head (Figs. 149b–d and 151c). Although the nostrils in the adult lamprey are unpaired, they do develop from paired olfactory pits (Johnels 1948; Mallatt 1996).

Chemosensory Faculty This is important for synchronizing sexual maturation, for reproductive behaviour, and for feeding. The system for collecting olfactory information has an ancient origin. However, amphioxus lacks an identifiable olfactory organ and its sensitivity to chemical stimuli remains unknown (Lacalli 2004). Pax6, a marker of the olfactory epithelium, is expressed only in the developing rostrum ectoderm (Glardon et al. 1998) and the dopaminergic neurons present

The Brain in the First Cristozoa: Evolutionary Origin of the Vertebrate Brain The centralization of the central neural system is characterized by the expansion of the anterior part of the neural cord, leading to the formation of the brain. The tripartite brain shares similar gene expression patterns across the major animal groups, suggesting that the tripartite gene expression ground plan arose very early.

Fig. 150 Pair of large eyes in Yunnanozoon lividum. (a) and (b) are counterparts of the nearly complete specimen, cf. Fig. 142A, B in its anterior part. Scale bar = 1 mm

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Fig. 151 Brain in Haikouella lanceolata from the Early Cambrian Maotianshan Shale. (a) a laterally compacted specimen showing side view of brain; (b, c) two dorso-ventrally compacted heads, showing ventrodorsal view of the brain.

Abbreviations: Dn, diencephalon; Hb, hindbrain; Sc, spiral cord; Va, ventral aorta; Da, dorsal aorta; En, endostyle; Ofb, olfactory bulb; Sn, snout; Ul, upper lip; Ma, mandibular aorta; Opn, optic nerves. (modified from Mallatt and Chen 2003). Scale = 1 mm

In contrast to the ancient origin of the tripartite gene expression ground plan, the nervous system might have centralized later (Lowe et al. 2006; Chen 2008, 2009), independently among the Deuterostomia, Ecdysozoa, and Lophotrochozoa. A recent study of fossil arthropods has prompted the surprising suggestion that the tripartite brain is not ancient at all (Chen 2009). The brain in the first arthropods (known as “proarthropods”) has only two divisions (Waloszek et al. 2005), corresponding to the protocerebrum and deuterocerebrum (Chen 2009). The tritocerebrum brain is a derived character and did not arise until the evolution of the euarthropods. The tripartite brain is also not an old structure in the deuterostomes. The deuterostomes, such as the echinoderms and hemichordates, have no brain at all. The nervous system might not have become centralized until the emergence of the chordates. In the tunicates and cephalochordates, the brain is not only very small but also incomplete. In the living cephalochordate amphioxus, the anterior part of the nerve cord

is weakly expanded; the minimally enlarged part has been described as a “cerebral vesicle” and shown to be morphologically and micro-anatomically different from the rest of the nerve cord (Fig. 147c). The “cerebral vesicle” can be divided into an anterior and a posterior part, with infundibular cells lying between the two subdivisions. The posterior termination is defined by the posterior end of the lamellar body. The cerebral vesicle embeds structures such as the front eye, lamellar cells, and infundibular cells; these may have homologues in the vertebrates occurring within the diencephalon (Lacalli et al. 1994; Lacalli 1996). The expression patterns of AmphiOtx (Williams and Holland 1998) and AmphiDll (Holland et al. 1996) agree well with the conclusions drawn from microanatomical studies (Lacalli et al. 1994). It is possible that the cerebral vesicle may also include a homologue of the vertebrate midbrain (Holland and Holland 1998), but there is no micro-anatomical support for this hypothesis. If a midbrain homologue exists at all in amphioxus, Lacalli et al. (1994) prefer to locate it

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behind the cerebral vesicle. The expression domain of the Pax 2/5/8 genes is widely considered to be a molecular marker for the MHB organizer. Although the AmphiPax2/5/8 genes are expressed in amphioxus, they are not expressed at the right site (Krešlová et al. 2002). The Pax2/5/8 genes are also expressed in ascidians, but the area of expression in the ascidians does not function as the MHB organizer in the vertebrates. All these data suggest that the MHB organizer is a novelty in the vertebrates and was not yet established in the protochordate evolutionary stage. Dmbx1 (a PRDclass homeobox gene) is one of the molecular markers of the vertebrate midbrain; it is expressed in the presumptive midbrain in the early developmental stages and in the hindbrain in later stages. In amphioxus, no Dmbx expression is observed in the neural tube. In the ascidian Ciona, the CiDmbx gene is detectable, but is not expressed in the presumptive midbrain in the early developmental stages, expressed instead in a region caudal to the Pax2/5/8-positive cells, in the anterior Hox region (Takahashi and Holland 2004). In summary, the evidence indicates that the protochordates lack a midbrain homologue. Based on gene expression patterns, the posterior limit of the region homologous to the forebrain+midbrain (Holland and Holland 1998; Shimeld and Holland 2000, 2005) lies at the level of the boundary between somites 2 and 3 in amphioxus, and the homologue of the posterior hindbrain lies at the boundary between somites 4 and 5 (Holland et al. 1992); the latter interval yields very little information about the anatomical counterpart within the vertebrate hindbrain. The transcription factor Krox-20 is an important molecular marker of the vertebrate hindbrain. However, a Krox-20-related gene, AmphiKrox, in amphioxus is expressed in different developing regions, including the anterior cerebral vesicle and a club-shaped gland, but its expression does not overlap with the expression domains of AmphiHox-1, -2, -3, and -4. The roles of Krox-20 in hindbrain segmentation and hindbrain development have not yet been established in amphioxus (Knight et al. 2000). Considered together, the evidence suggests that the hindbrain is absent in amphioxus and that its brain contains only a homologue of the vertebrate diencephalon. The fabulously preserved outlines of the brain in Haikouella provide novel evidence of the ground plan of the cristozoan brain (Figs. 149a–b and 151). The brain occurs as a conspicuous enlargement of the front

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part of the spinal cord on the dorsal side of the pharynx (Figs. 149a–b and 151a). It is about 4 mm long, 0.4 mm thick, and 0.5 mm wide and is much larger (relative to its body size) than that in amphioxus (Fig. 147c), but equal in size to those of other vertebrates, including the jawless and bony fishes, amphibians, and reptiles. It contains two morphological parts, with the boundary line drawn dorsally straight from the ventral part of the mandibular artery. The brain posterior to the line is interpreted as the hindbrain (Mallatt and Chen 2003) and occurs as a posterior narrowing of the brain, with its end at the third (vagal) branchial bar, situated exactly at the same position as in the jawless craniates (Figs. 149b and 151a; Mallatt and Chen 2003). The brain anterior to the line is an elongated and bulbous feature. Dorsoventrally compacted specimens of the anterior part of the brain (Fig. 151b, c) confirm the absence of large, paired, cerebral hemispheric structures related to the telencephalon, except for a pair of small bulges that are interpreted as olfactory nerves (or bulbs; about 0.1 mm thick). The anterior part has a pair of lateral eyes embedded at its rear end; these are homologous to the diencephalon. It is about 1 mm long, 0.3–0.4 mm thick (Fig. 151a), and 0.5 mm wide. The front margin of the brain in Haikouella resembles that of amphioxus and the brains in both do not reach the front margin of the head, but end at a position about 1.5 mm from the front margin in Haikouella (Figs. 149b and 151a) and at a rear part of the rostrum, about 0.5 mm from the anterior margin, in amphioxus (Fig. 147c). Deuterostomes, such as the echinoderms and hemichordates, have no brain. The centralization of the deuterostome nervous system most likely evolved in the common ancestor of the chordates, with the occurrence of the first visible but miniature simple brain in the protochordates, as seen in extant cephalochordates and tunicates. The brain ground plan in the chordates, exemplified in the extant protochordate tunicates and cephalochordates, is not only small but also compact and incomplete, and its possible vertebrate homology lies basically within the diencephalon, in both tunicates (Lacalli and Holland 1998) and cephalochordates (Lacalli et al. 1994; Lacalli 1996). However, there is little or no morphological evidence for homologues of the vertebrate telencephalon, midbrain, or hindbrain. Brain evolution during the pre-cristozoan-tocristozoan transition might have been triggered by an increasingly active lifestyle and was marked by the

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

expansion and rearward extension that led to the formation of a morphologically recognizable hindbrain. The brain ground plan in Cristozoa, as exemplified by Haikouella, is a relatively large and elongated structure consisting of two morphologically distinct parts, homologous to the craniate diencephalon and hindbrain. A possible midbrain might lie between the diencephalon and the hindbrain. Compared with the size of the brain in the cephalochordate amphioxus, the brain in the first cristozoans, as exemplified by Haikouella, is extremely large, although amphioxus and Haikouella are the same size. There is no morphologically recognizable telencephalon homologue in the first Cristozoa. Whitlock and Westerfield (2000) demonstrated that the olfactory nerves are closely related to the telencephalon during embryonic development. The presence of possible paired olfactory nerves (or bulbs) in Haikouella (Fig. 151b, c) implies that the olfactory nerves (or bulbs) are the precursors of the telencephalon. The emergence of a morphologically clear telencephalon is a novelty in the craniates. The anterioposterior gene expression patterns along the dorsal nerve cord in ascidians and vertebrates share a similar basic tripartite ground plan, comprising an anterior Otx expression region (the forebrain and midbrain in the vertebrates), a Pax2/5/8-expressing central region (MHB), and a Hox-expressing region (hindbrain and spinal cord in the vertebrates; Takahashi and Holland 2004). A similar tripartite gene expression pattern appears in the non-chordate deuterostomes, the hemichordates (Lowe et al. 2006), and the arthropods (Hirth et al. 2003) suggesting that the tripartite gene expression ground plan arose very early, even before the evolution of the chordates, from the common ancestor of the protostomes and deuterostomes. In contrast to the ancient origin of the tripartite gene expression ground plan, the nervous system might have centralized later (Lowe et al. 2006), independently among the Deuterostomia, Ecdysozoa, and Lophotrochozoa.

Branchial System in the Cristozoan Ground Plan Water is 800 times denser than air and the dissolved oxygen in water is 30 times more dilute than in air. The cost of respiration is rather high, accounting for

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up to 30% of the total metabolic energy (Young 1981). The adaptations for a more active lifestyle that evolved during the transition from an amphioxus-like ancestor towards the crest animals very probably demanded an increased metabolic rate. The replacement of the gill-less pharyngeal system with a gill-based pharyngeal system and the change in the ventilation mechanism from ciliary to muscular are two of the major landmarks in the transition from an amphioxuslike ancestor to the crest animals, as predicted by Northcutt and Gans (1983).The change allowed a more active lifestyle in terms of feeding, oxygen intake, and locomotion, with an increasing metabolic rate. In the ancestral gill-less pharyngeal system, as exemplified by amphioxus, water is pumped through the pharynx by cilia on the branchial arches and these cilia-bearing arches must be arranged close to each other to form narrow, regularly spaced, branchial slits (Fig. 152a). The secondary growth of new additional branchial arches in later developmental stages, with the larger numbers of closely spaced branchial arches in the adult, characterizes an ancestral gill-less pharyngeal system. The gill-less branchial arches do not function in oxygen uptake (Schmitz et al. 2000), but are used for food intake. The gill pharyngeal system is a novelty of the crest animals. When the gill-less ancestor became a more active swimmer, the increased metabolic rate required must have triggered the selection of animals with a more efficient respiratory system, and thus the development of gills and gill rays (gill-supporting structures). The development of gills with increasing resistance to water flow might have prompted an evolutionary change from ciliary ventilation to the more powerful, muscular ventilation pump and the replacement of the thin, unjointed branchial arches with thicker, segmented, cartilagenous branchial arches. These are stronger and more capable of the elastic recoil that expands the pharynx to draw in water during inhalation. Fewer, more widely spaced branchial arches, as exemplified in Haikouella (Fig. 152e–g) and Yunnanozoon (Fig. 152h), would reduce the resistance to the water flow passing under the pressure of muscular ventilation, characterizing the transition from the amphioxus-like ancestor to the crest animals. It was argued by Mallatt in 1996 that the common ancestor of the craniates had both internal and external branchial arches, as observed in the anterior pharynx of the living hagfish Myxine glutinosa (Holmgren 1946).

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Fig. 152 Branchial system in living Cephalochordata (a, b), Urochordata (c, d) and Early Cambrian Cristozoa (e–h). A, view from right side of Branchiostoma belcheri showing closely arranged branchial arches; (b) enlargement showing closely arranged branchial arches and synapticula between branchial arches; (c, d) living urochordates showing closely arranged branchial arches connected by transverse bars with gill-slits consistent in size; (e) showing segmented branchial arch with a

pair of gill rays in each segment in Haikouella; (e–g) Branchial system in Haikouella showing brachial manidibular aorta and branchial arches with paired gill rays; (h) branchial arches with paired gill rays in Yunnanozoon lividum. Abbreviations: Ma, mandibular aorta; Da, dorsal aorta; Va, ventral aorta. (h, reproduced by permission from D. Y. Huang). Scale bars = 2 mm (a, f–h), 200 μm (b), and 100 μm (e)

However, the adult lamprey has only unjointed, external branchial bars. The internal branchial arches are proposed to have been secondarily lost in the lamprey, whereas those in some other pre-gnathostomes were enlarged and subdivided into associated ventilation muscles (Mallatt 1996). The early Cristozoa, including Haikouella and Yunnanozoon, have only one set of branchial arches

with paired gill rays, interpreted by Mallatt and Chen (2003) to project externally from the branchial arches and thus to be homologous to the external branchial arches of the craniates. Further observation has shown that most of the intact gill rays in Haikouella project internally rather than externally from the branchial arches (Fig. 152f, g), and thus play a role similar to those of the internal branchial arches. The branchial

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

arches are segmented with joints, which might provide both the branchial arches and their gill-rays with the flexibility to allow the reorientation of the gill rays, to adapt to different levels of feeding activity. The paired gill rays can form a narrow angle and project posteriorly, with one placed within the pharyngeal lumen and the other outside the lumen but within the atrium (Fig. 154a). This suggests that the branchial arches in the early Cristozoa are homologous to the internal branchial arches in function, although they may have played roles in both internal and external functions in some cases. The branchial arches in both the cephalochordates (Fig. 152a, b) and tunicates (Fig. 152c, d) lie close together, maintaining very narrow branchial slits of a consistent size. As the animals become larger, they must add new branchial arches as they grow to meet the increasing ventilatory demands of filter feeding. The branchial arches are fairly thin, non-cellular structures usually connected to each other by fine transverse bars (called “synapticula” in amphioxus) that limit the size of the gill slits (Fig. 152b); the upper size limit of food particles is fixed by the size of the gill slits and includes microbes and phytoplankton. The transformation of an amphioxus-like invertebrate ancestor into the evolutionary line of vertebrate animals was probably driven by an increasingly active lifestyle and an increasingly higher metabolic rate, triggering a series of consequent changes in the branchial system. A central event in the changes was the shift from ciliary ventilation to respiratory muscular ventilation with gills (Northcutt and Gans 1983). The branchial arches of Haikouella and Yunnanozoon are not only broad but also segmented with joints, and each segment has a pair of thin, blade-shaped, skeletal gill rays (Fig. 152e–h; Chen et al. 1999; Mallatt and Chen 2003; Chen 2004; Chen and Huang 2006). The same structures occur in the bony fishes, in which they support the respiratory gill filaments and gill septa (Hughes 1984; Laurent 1984) and act as insertion sites for the branchiomeric muscles (Dunnel-Erb et al. 1993). The occurrence of gill rays, possibly with gills, in Haikouella and Yunnanozoon (Mallatt and Chen 2003) indicates that muscular ventilation was an early structure, representing a novelty in the crest animals. Paired gill rays are known only in the bony fishes, but are absent in the agnathans and primitive jawed fishes such as Chondrichthys. Chondrichthys has gill

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rays but they are larger and unpaired. The paired gill rays are not considered to be a primitive feature in the crest animals. However, the occurrence of paired gill rays in both Haikouella and Yunnanozoon suggests that paired gill rays are a primitive character, occurring at the very beginning of the crest animals, and that their absence in the agnathans is ascribable to secondary degeneration. Alternatively, these early gill rays may not be homologous to those of the bony fishes (Mallatt and Chen 2003). The respiratory muscular ventilation in Haikouella and Yunnanozoon is confirmed not only by gill bars but also by the branchial arches, which are robust, jointed, bendable, and presumably capable of elastic recoil. They are fewer in number, with wider slits (or pouches) to lower the resistance to the water flow passing under the pressure of muscular ventilation (Mallatt and Chen 2003). The branchial arches in Haikouella are about 120 μm in diameter, slightly thicker than those in the living larval sea lamprey, but much thicker than those of amphioxus, although they have similar body sizes. The branchial arches measure about 80 μm in diameter in the larval sea lamprey, but only 30 μm in amphioxus. They are abundantly jointed and consist of numerous stacked discs, resembling those of the branchial arches made by cartilage cells in the larval lamprey and embryonic fishes (Pardos and Benito 1988; Kimmel et al. 1998; Holland and Chen 2001; Mallatt and Chen 2003), suggesting the branchial arches to be cellular, composed of cartilage. Cartilage and multijointed branchial arches are novelties in the Cristozoa (Meulemans and Bronner-Fraser 2007). There are few branchial arches in the early developmental stages of protochordates (including the cephalochordates and tunicates) and hemichordates in their early developmental stages, but they increase in number as the animal grows. In contrast, the vertebrates not only have much fewer branchial arches (usually no more than seven) but they also always lack secondarily derived branchial arches, appearing only in later development (Jefferies 1986; Mallatt and Chen 2003; Chen 2008). A small but constant number of branchial arches is a novelty of the Cristozoa and presumably represents a larval version of the pre-Cristozoa ancestor, resulting from a paedomorphic process (Chen 2008). There are fewer than ten branchial arches in all the crest animals, with the exception of the agnathans,

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with usually up to 15 branchial arches (or pouches) in the living hagfishes and 45 in the fossil hagfishes (Janvier 2004). However, the early crest animals, as exemplified by Haikouella and Yunnanozoon, have only six post-mandibular arches, plus the mandibular arch. Interestingly, the mandibular arch is absent in Haikouella but is represented by the mandibular artery (Fig. 152g; Mallatt and Chen 2003), suggesting that the vertebrate branchial arches did not arise synchronously and that the mandibular arch is a structure slightly younger than the other branchial arches. There are seven pairs of branchial arches in Yunnanozoon (Fig. 145b, c); this is probably the prototype of the crest animals. More than seven branchial arches, as seen in the agnathans, is a secondarily derived character.

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branchial slits of the pharyngeal lumen and convey it to the outside through the atriopore in the cephalochordates (Fig. 147b) or through an exhalent siphon in the tunicates. The atria might function to protect the delicate branchial arches from muddy and sandy substrata during swimming and burrowing (Holland and Chen 2001) and to protect the delicate gill rays from damage by water currents during swimming. The atria are present in amphioxus but absent in the craniates, although they are still present in the early crest animals, as exemplified by Haikouella (Fig. 153a) and Yunnanozoon, suggesting that the early crest animals were capable of burrowing temporarily into the soft mud when the animal encountered a predator.

Endostyle Atria The pharynx of the early crest animals, as represented by Haikouella and Yunnanozoon, is protected by a pair of water chambers known as “atria”, indicated by the presence of an atrial pore and its related mud-filled cavity (Fig. 153a) and by the mud-filled atrial chamber in a dorsoventrally compacted specimen. These atria are a plesiomorphic character and also occur in the protochordates, including the ascidians and cephalochordates, but disappear in the craniates. They represent water chambers on the sides of the pharynx, receiving the exhalent ventilation water leaving the

The thyroid gland is a craniate-only character and one of the largest endocrine glands in the group. It produces thyroid hormones, principally thyroxine (T4) and triiodothyronine (T3), to regulate the rate of metabolism and affect the growth and rate of function of many other body systems. The endostyle is the precursor of the craniate thyroid gland, producing both thyroid and digestive glands, and adding mucus and digestive enzymes to trapped food grains in the pharynx during suspension feeding. The mucoproteins contain monoiodothyronine (T1), diiodothyronine (T2), T3, and T4, perhaps regulating the metabolic rate and

Fig. 153 Pharyngeal teeth (marked with arrows) in Haikouella lanceolata (a, b) and Yunnanozoon lividum (c, d) from the Early Cambrian Maotianshan Shale. Scale bars = 5 mm (a, c, d) and100 μm (b)

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

affecting the growth and functions of body systems, as in vertebrates. However, T3 is relatively more abundant in amphioxus. The endostyle is an evolutionary precursor of the thyroid gland and occurs as a longitudinal ciliated groove on the ventral wall of the pharynx, producing mucus to gather food particles and to assist in transporting food to the oesophagus. The endostyle is a chordate-only structure; it is present in the protochordates (including the cephalochordates and urochordates) and existed continuously in the early crest animals, as exemplified by Yunnanozoon (Fig. 153d) and Haikouella (Figs. 151a, b and 152g). In some living primitive craniates, such as the lamprey, the endostyle remains in the larval stage only (Barrington and Sage 1972), suggesting the thyroid gland to be an evolutionary novelty in the craniates.

Pharyngeal Teeth Simple cone-shaped denticles occur on the pharyngeal floor in Yunnanozoon and Haikouella (Chen et al. 1999; Holland and Chen 2001) making it a possibility for the teeth to be evolutionarily deeply rooted, representing an apomorphic character in the Cristozoa that emerged before the onset of the mineralized dermal skeleton. The teeth in the early cristozoans, as exemplified by Haikouella and Yunnanozoon, are simply coneshaped, situated on the pharyngeal floor (Fig. 153). The teeth in Haikouella are small (only 0.1 mm), located medially on the floor of the pharyngeal cavity (Fig. 153a, b), but they are much larger (about 1 mm each) when situated at the rear of the pharynx in Yunnanozoon (Fig. 153c, d). The pharyngeal teeth are probably a primitive feature in the cristozoans and are also present in conodont animals. Pharyngeal teeth that predate the origination of skin scales challenge the scale-origination hypothesis of teeth evolution (Romer 1962). When larger food grains entered the pharynx, animals used the intra-pharyngeal denticles to pierce and break them down before they entered the gut (Chen et al. 1999; Holland and Chen 2001; Mallatt and Chen 2003). The small (only 0.1 mm) intra-pharyngeal denticles in Haikouella are probably allowed food particles of up to 0.3 mm to be processed. Food may have included embryos and larvae. The much larger (1 mm) intra-pharyngeal denticles of Yunnanozoon

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suggest that the animal was able to feed on food items larger than 1 mm, up to 3–4 mm, including embryos and small animals such as bradoriids, Ercaia, and Primicaris (Chen 2004). These food animals were not only small (in the range of 2–4 mm for bradoriids and Ercaia and 1–7 mm for Primicaris) but were also extremely abundant in the Maotianshan Shale fauna.

Evolution of the Axial Skeleton The notochord is an axial, non-bony, hydrostatic skeleton and a chordate-only character. The notochord appears only in the tail of the larval stages of the tunicates but remains well developed throughout life in the cephalochordates. In the cephalochordates, the notochord is a large, distinct structure, extending throughout the entire length of the body (Fig. 147a, b). The notochord exists in vertebrates, but it tends to degenerate, and is reduced or almost entirely lost in the adult form. The protochordates burrowed in clean sand, as demonstrated by the living amphioxus. Its body tapers to a point at both the anterior and posterior ends, allowing the animal to push aside sand with either the head or tail end first while burrowing. These burrowing activities may have triggered the emergence of the axial skeleton, known as the “notochord”, allowing the animal to resist deformation when burrowing in the sand, either head or tail first (Fig. 148). The notochord of amphioxus is the living representative of the first axial skeleton, extending to both body termini. The function of the early axial skeleton was not only to resist axial deformation while burrowing but also for the attachment of the muscles used in burrowing or while swimming with a burst of rapid lateral undulations of the body. The notochord exists in the vertebrates, but they have also developed a novel axial skeleton known as the “vertebrae”, bony elaborate joints, encasing both the notochord and spinal cord. The bony vertebrae have made the soft notochord superfluous, degenerating in the adult until it was almost entirely lost. The notochord in the Cristozoa ground plan, as exemplified by Haikouella and Yunnanozoon, resembles the large and distinct structure of amphioxus. Unlike that in amphioxus, the notochord of Haikouella disappears anteriorly at about the dorsal location of branchial

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Fig. 154 Laterally compressed Haikouella lanceolata from the Early Cambrian Maotianshan Shale showing protovertebrae (a– c), notochord (a, b), brain (a), posteriorly directed gill rays (a), four pairs of gonads (b, c), atrium (b, c), intestine (b, c), anus

(b), tail (b), mouth (a). Red arrow represents the dorsal margin of protovertebrae; blue arrow indicates dorsal margin of notochord. Scale bar = 5 mm

arch 3, whereas in amphioxus, it extends continuously to the anteriormost end of the body. The vertebral column is a vertebrate-only character. Its origin remains controversial, and it was thought to be a younger structure than the skull. Haikouella and Yunnanozoon have segmented cartilagenous structures (Fig. 154) that represent the precursor of the vertebral column of advanced vertebrates and are comparable to the protovertebrae in the living lamprey (Chen and Li 2000; Holland and Chen 2001; Young

1981), suggesting that the vertebrae evolved before the origination of the elaborated skull.

Musculoskeleton Myotomes are divided by myosepta (or myocommata) into repeated, segmented structures known as “myomeres” (muscle segments). These are a chordate-only character, present only in the extant

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Fig. 155 Musculature in the first crest animals Haikouella lanceolata (a, b) and Yunnanozoon lividum (d, e) and in the extant cephalochordate Branchiostoma belcheri (c) showing

myocommata (a–e), myomeres with muscle fibres (a–e), and skin on top of both the myomeres and myocommata (d, e). Scale bar = 0.5 mm (a, c) and 5 mm (b, d–e)

cephalochordates, craniates, and larval tunicates. In these taxa, the myosepta have a complex V- or Wshape. In Haikouella and Yunnanozoon, there are about two dozen myomeres, separated by myosepta in a simple straight form (Fig. 155), as in the young larvae of the living cephalochordates and tunicates. Because of their unusual simplicity and dorsal location, they were regarded as a large, segmented fin by Shu et al. (1996) and as cuticular rings by Conway Morris (2000). The preservation of the muscle fibres in some Haikouella specimens (Fig. 155b, c) and the muscle fibres and wrinkled skin overlying the muscles in some Yunnanozoon specimens (Fig. 155c, d) confirm that these segmental structures are truly myomeres (Chen and Li 1997; Mallatt and Chen 2003). The young larvae of lancelets (Fig. 155c) and tunicates have the same simple, straight, segmental muscles and swim well (Holland and Chen 2001). Simple myosepta may represent the ground plan of the crest animals. The presence of W-shaped myosepta in the Lower Cambrian Haikouichthys (Shu et al. 1999b) indicates that the W-shaped myosepta had a very early origin, evolving independently and directly from the simple straight form at an advanced evolutionary stage of

the precraniates or at the beginning of the evolutionary history of the craniates. The complex V-shaped myosepta in the cephalochordates and the W-shaped myosepta in the crest animals presumably represent parallel evolution. Positional relationships of the musculoskeletal structure, the axial skeleton, the neural cord, and the branchial structure among the chordates are confused. The “dual animal” hypothesis of Romer (1972) proposed that the vertebrates evolved from a tadpole larva-like ancestor, in which the body was segregated into a visceral head and a somatic trunk. Romer’s hypothesis pushes tunicates to the central stage of vertebrate origins. However, the ascidian body plan is so derived that in some respects it is not very useful; for discussion of the origin of the vertebrate body plan, see Lacalli (2005). Amphioxus and Haikouella display an anterior– posterior body organization that is very different from that of the “dual animal” of Romer. In amphioxus, the musculoskeletal structure extends anteriorly at a level corresponding to the rostral margin of the cerebral vesicle (a homologue of the vertebrate diencephalon), whereas the rostral margin in Haikouella lies at a level

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corresponding to the possible MHB in the vertebrates. That the visceral head and somatic trunk in both the amphioxus-like pre-cristozoan ancestor and the early crest animals were not segregated but integrated is a possibility.

Evolution of Feeding Behaviours As predicted by many authors, changes in feeding behaviour evolved with the changes in ventilation, before any true predator arose (Northcutt and Gans 1983; Mallatt 1996; Purnell 2001). The change in feeding behaviour during the transition from an amphioxus-like ancestor towards the crest animals, as exemplified by Haikouella and Yunnanozoon, is marked by the ability to handle increasingly larger food items before a true predator arose. The maximal food size of these early crest animals ranged from about 300 μm to a few millimetres. The emergence of elaborate olfactory organs, as exemplified in Haikouella, allowed these early crest animals to become selective feeders on food with higher nutritional value, probably including the embryos, immobile larvae, and small invertebrates available on the seafloor. The large muscular upper lips of the early crest animals could form an oral hood to drape over a cluster of interesting food items on the sea bottom, and their muscular ventilation allowed the animals to then suck the prey items through the mouth into the pharynx.

Evolutionary Tree of the Deuterosomes and the Approach Towards a Backbone Although the deuterostomes are a morphologically well-defined group and probably monophyletic, there is no agreement about the shape of their evolutionary tree. Figure 156 suggests that the deuterostomes derived from a tentaculate worm-like ancestor (1) in two basic branches: the tentaculate deuterostomes (11) and the living pharyngeal deuterostomes (2). Tentaculate feeding was presumably the plesiomorphic character of the deuterostomes. Phlogites (12) from the Lower Cambrian Maotianshan Shale, with least complexity, probably represents the ancestral form of the tentaculate sessile deuterostomes. Phlogites exemplifies the ground plan of the tentaculate deuterostomes insofar as it is sessile and characterized by a spacious

J.-Y. Chen

cavity that encloses a coiled gut (12). A set of large hollow and branched tentacles surrounding the mouth forms a feeding bowl. The anus is situated close to the mouth but outside the feeding bowl. From a Phlogites-like ancestor (13), the two major tentaculate deuterostome branches arose: the phoronids+brachiopods (14, 16) and the eldoniids+echinoderms (19). The phylogenetic positions of both the Brachiopoda and Phoronida remain controversial. Molecular studies exclude the brachiopods from the deuterostomes and both Brachiopoda and Phoronida are usually interpreted as protostomes. However, they share a number of characters unique to the deuterostomes (Nielsen 2001). Phoronida has a secreted chitinous tube (15) and Brachiopoda has mineralized dorsal and ventral valves (16). The eldoniid+echinoderm clade (17) is characterized by a highly developed water-vascular system that includes radial canals, a central ring, and tubular outgrowths of the body wall (tube feet). This clade is adapted for two different lifestyles, a pelagic lifestyle in the eldoniids (18) and a sessile lifestyle in the echinoderms (19). Pharyngeal feeding, with the related branchial slits, is an apomorphic character in the deuterostomes. The hemichordates (3) lie at the evolutionary base of the pharyngeal deuterostome clade, representing different evolutionary stages in the transition from tentaculate feeding to pharyngeal feeding. Among the extant hemichordates, the pterobranchs are predominantly tentaculate feeders, except for Cephalodiscus. With a single pair of gill slits, these represent the early evolutionary history of pharyngeal feeding. Enteropneusts (= acorn worms) are all pharyngeal feeders, representing an advanced evolutionary stage of the hemichordates. The enteropneust body is characterized by an anterior proboscis, a small middle collar, and a long posterior trunk. The animal uses its muscular proboscis for burrowing with retrograde peristaltic waves that transport the sand rearward. The Chordata (4) is the sister group of the Hemichordata (3); both groups are adapted for burrowing, but in different ways. Unlike the hemichordate enteropneusts, which use a muscular proboscis for burrowing, the first chordates (5), exemplified by the extant amphioxus, developed a lancelet-like body that narrows to a point at both ends, burrows with the help of an axial skeleton (notochord). The ground plan of the notochord in chordates, as exemplified by

Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian . . .

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Fig. 156 Phylogenetic kinship of the high ranking clades among the Deuterostomata. (1) tentaculated worm-like ancestor; (2) evolutionary origin of the pharyngeal deuterostomes; (3) Hemichordata representing the transitional stage from tentaculate feeding to pharyngeal feeding; (4) Chordata with key novelties including axial skeleton (notochord), musculature system and centralization of central nerve system; (5) cephalochordates, the stem group of the Chordata; (6) evolutionary origin of the Urochordata+Cristozoa clade; (7) Urochordata (adapted for an inactive lifestyle); (8) Cristozoa (adapted for a more active lifestyle) marked by key novelties including whole genome duplication, neural crest cells and related producers, protovertebrae, gill-pharyngeal system, muscular ventilation system, brain size expansion, image-forming lateral eyes, and possible nostrils; (9) Procraniata representing the stem lineage of Cristozoa; (10) craniate cristozoans marked by presence both

of a complex skull and telecephalon. (11) origin of tentaculate deuterostomes; (12) Phlogites-like animals (characterized by a spacious cavity enclosing a coiled gut; a set of large hollow and branched tentacles surrounding the mouth forms a feeding bowl (anus is situated close to the mouth but outside of the feeding bowl); it represents the stem lineage of the tentaculate deuterostomes; (13) origin of advanced tentaculate deuterostomes; (14) origin of common ancestor of the phononids+brachiopod clade; (15) Phoronida (having a secreted chitinous tube); (16) Brachiopoda characterized by mineralized dorsal and ventral valves; (17) origin of common ancestor of eldoniid+echinoderm clade—characterized by a highly developed water-vascular system including radial canals, central ring, and tubular outgrowths of the body wall (the tube feet); (18) eldoniids (adapted for a pelagic lifestyle); (19) echinoderms (adapted for a sessile lifestyle)

amphioxus, is large, extending the entire length of the body. The notochord plays a role not only in resisting axial deformation under stress while the animal burrows through sand, either head or tail first, but also in muscle attachment while the animals burrow or swim with bursts of rapid lateral undulations of the body. The early Cristozoa (9) are soft bodied; predatory avoidance behaviour was critical to their survival— burrowing is one of the behaviours used to avoid predation. Development of the fast-start response is another major predation-avoidance behaviour in which the body accelerates rapidly from a perceived threat. The complex musculature plays a critical role in the fast-start response, as seen in all fishes today (Westneat et al. 1998). The Cristozoa+Urochordata clade (6) arose from an amphioxus-like ancestor and branched dichotomously into two groups, the urochordates (7) and the crest animals (8) at a time before the first round of whole-genome duplication in the vertebrates. The Urochordata is probably the sister group of the Cristozoa and diverged from the evolutionary lineage leading to the latter before the whole-genome duplication event. The origin of the Urochordata (7)

was presumably driven by selection pressure that adapted them to an inactive sessile lifestyle. They not only diverged morphologically from the main evolutionary pathway to the Cristozoa, but their genome displays substantial reduction, contrary to the expansion observed in Cristozoa. The transition from an amphioxus-like ancestor to the Cristozoa (8) was probably triggered by selection pressure for a more active lifestyle. The evolutionary key novelties that led to the transformation of the amphioxus-like ancestor to the Cristozoa included whole-genome duplication, neural crest cells and related producers, protovertebrae, the gill–pharyngeal system, the muscular ventilation system, brain expansion, image-forming lateral eyes, and possible nostrils. The transition from the procraniate cristozoans (9) to the craniate cristozoans (10) was marked by the clearly complex skull and telencephalon. Molecular and morphological evidence unite the hemichordates and echinoderms as the Ambulacraria, but their earliest history remains almost entirely conjectural. This is on account of the morphological disparity of the ambulacrarians and a paucity of obvious stem-groups. We describe here a new taxon

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Herpetogaster collinsi gen. et sp. nov. from the Burgess Shale (Middle Cambrian) Lagerstätte. This soft-bodied vermiform animal has a pair of elongate dendritic oral tentacles, a flexible stolon with an attachment disc, and a re-curved trunk with at least 13 segments that is directed dextrally. A differentiated but unlooped gut is enclosed in a sac suspended by mesenteries. It consists of a short pharynx, a conspicuous lenticular stomach, followed by a narrow intestine sub-equal in length. This new taxon, together with the Lower Cambrian Phlogites and more intriguingly the hitherto enigmatic discoidal eldoniids (Cambrian-Devonian), form a distinctive clade (herein the cambroernids). Although one hypothesis of their relationships would look to the lophotrochozoans (specifically the entoprocts), we suggest that the evidence is more consistent with their being primitive deuterostomes, with specific comparisons being made to the pterobranch hemichordates and pre-radial echinoderms. On this basis some of the earliest ambulacrarians are interpreted as softbodied animals with a muscular stalk, and possessing prominent tentacles. Acknowledgments This work was supported by the National Basic Research Program of China (grants 2007CB815800 and 2006CB806400) and the National Science Foundation of China (grant 41023008). I thank John Talent, editor of this volume, for helpful comments and polishing the English of the manuscript; he and several assessors, including SQ Dornbos, Ruth Mawson, Peter Cockle, Janine Miller, and Karen Novotny, also contributed importantly to editing of the manuscript. Technical assistance was given by HZ Wu and XZ Li. This paper presents a wide coverage of research advanced by stimulating collaboration and discussion with many colleagues and former students, especially E Davidson, D Bottjer, MG Hadfield, L Gang, F Gang, and P Tafforeau on the Weng’an biota; J Mallat, D Waloszek, A Maas, MY Zhu, DY Huang, SQ Dornbos, J Vannier, N Holland, and SH Chuang on the Maotianshan Shale biota.

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